Reconstructing the ancestral angiosperm flower and its initial specializations

22

American Journal of Botany 96(1): 22–66. 2009.

The question of the structure and biology of the ancestral angiosperms, and especially their fl owers, is an enduring riddle. Although we are continually gaining new insights from new fossils and new studies on phylogeny, morphology, and devel-opmental genetics in extant plants, we are still far from a fi nal answer. There are gaps at different levels. First is the uncer-tainty concerning which other seed plants are the closest rela-tives of angiosperms, particularly extinct groups because most molecular analyses indicate that no living group of gymno-sperms is any closer to angiosperms than any other. Second, even if known fossils can be recognized as angiosperm stem relatives, all such groups are morphologically well removed from angiosperms, so there is still a major gap that can only be fi lled by the discovery of closer stem relatives. Third is the problem of the original morphology and early evolutionary dif-ferentiation of crown group angiosperms.

Identifi cation of seed plant relatives of the angiosperms has been one of the most contentious issues in plant systematics and evolution, both before and after the introduction of phyloge-netic methods ( Crane, 1985 ; Doyle and Donoghue, 1986 ; Nixon et al., 1994 ; Doyle, 1994 , 1996 ). Molecular analyses contradict one of the few points on which morphological analyses agreed, that Gnetales are the closest living relatives of angiosperms ( Donoghue and Doyle, 2000 ; Burleigh and Mathews, 2004 ; Soltis et al., 2005 ), but they say nothing about fossil relatives. Several recent studies, some of which take into account mo-

lecular results, have linked glossopterids, Pentoxylon , Bennet-titales, and Caytonia , with or without Gnetales, with angiosperms ( Bateman et al., 2006 ; Doyle, 2006 ; Friis et al., 2007 ; Frohlich and Chase, 2007 ), but there is no general agreement that any of these taxa are related to angiosperms. The question of still closer angiosperm stem relatives is still a void because there are no fossils that undisputedly represent this part of the tree.

Fortunately, there has been much more progress in recon-struction of the fi rst crown group angiosperms. Recent work on early fossil angiosperms (reviewed by Doyle, 2001, and Friis et al., 2006 ) and on extant “ ANITA grade ” angiosperms ( Endress, 2001 , 2008a) has provided new insights. Problems at this level have become easier to tackle thanks to analyses of liv-ing angiosperms, particularly using molecular data, which have clarifi ed relationships within the crown group with a degree of precision and statistical confi dence barely imaginable two de-cades ago. These analyses have consistently rooted the an-giosperm phylogenetic tree among the ANITA lines, namely Amborella , Nymphaeales, and Austrobaileyales ( Mathews and Donoghue, 1999 ; Parkinson et al., 1999 ; Qiu et al., 1999 ; Renner, 1999 ; Soltis et al., 1999, 2000 ; Barkman et al., 2000 ; Graham and Olmstead, 2000 ; Zanis et al., 2002 ), which has focused at-tention on these taxa as particularly likely to yield insights on the fi rst angiosperms ( Doyle and Endress, 2000 ; Endress and Igersheim, 2000a , b ; Endress, 2001 , 2004 , 2006, 2008a; Fried-man and Williams, 2003 , 2004 ; Williams and Friedman, 2004 ; Friedman, 2006 ; Endress and Doyle, 2007 ). The main uncer-tainty is whether Amborella and Nymphaeales form two succes-sive branches or a clade ( Barkman et al., 2000 ), with some recent support for the latter hypothesis from mitochondrial genes ( Qiu et al., 2006 ), but the former supported by recent analyses of entire plastid genomes ( Jansen et al., 2007 ; Moore et al., 2007 ). An alternative rooting based on plastid genomes of fewer taxa, with grasses the sister group of all other angiosperms ( Goremykin et al., 2003 ), appears to be an artifact of low taxon sampling and long branch attraction ( Degtjareva et al., 2004 ; Soltis and Soltis, 2004 ; Stefanovic et al., 2004 ; Leebens-Mack et al., 2005 ).

1 Manuscript received 7 February 2008; revision accepted 12 September 2008. The authors thank E. M. Friis and M. Frohlich for useful discussions and

suggestions that improved the manuscript. J.A.D. thanks P. Garnock-Jones and the School of Biological Sciences, Victoria University of Wellington, for facilities and a supportive environment during preparation of this paper. This work was facilitated by travel support from the NSF Deep Time Research Coordination Network (RCN0090283).

4 Author for correspondence (e-mail: [email protected])

doi:10.3732/ajb.0800047

RECONSTRUCTING THE ANCESTRAL ANGIOSPERM FLOWER AND ITS INITIAL SPECIALIZATIONS 1

Peter K. Endress 2,4 and James A. Doyle 3

2 Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland; and 3 Department of Evolution and Ecology, University of California, Davis, California 95616 USA

Increasingly robust understanding of angiosperm phylogeny allows more secure reconstruction of the fl ower in the most recent common ancestor of extant angiosperms and its early evolution. The surprising emergence of several extant and fossil taxa with simple fl owers near the base of the angiosperms — Chloranthaceae, Ceratophyllum , Hydatellaceae, and the Early Cretaceous fossil Archaefructus (the last three are water plants) — has brought a new twist to this problem. We evaluate early fl oral evolution in an-giosperms by parsimony optimization of morphological characters on phylogenetic trees derived from morphological and molecu-lar data. Our analyses imply that Ceratophyllum may be related to Chloranthaceae, and Archaefructus to either Hydatellaceae or Ceratophyllum . Inferred ancestral features include more than two whorls (or series) of tepals and stamens, stamens with protrud-ing adaxial or lateral pollen sacs, several free, ascidiate carpels closed by secretion, extended stigma, extragynoecial compitum, and one or several ventral pendent ovule(s). The ancestral state in other characters is equivocal: e.g., bisexual vs. unisexual fl owers, whorled vs. spiral fl oral phyllotaxis, presence vs. absence of tepal differentiation, anatropous vs. orthotropous ovules. Our results indicate that the simple fl owers of the newly recognized basal groups are reduced rather than primitively simple.

Key words: ancestral fl owers; angiosperm phylogeny; ANITA grade; Archaefructus ; basal angiosperms; Ceratophyllum ; Chloranthaceae; fl ower evolution; Hydatellaceae; water plants.

23January 2009] Endress and Doyle — Ancestral flowers

could be said to be typical at a relatively “ basal ” level of angio-sperms (groups other than monocots and eudicots, or “ Magno-liidae ” in the paraphyletic sense of Takhtajan, 1964 ), but because they were scattered in different taxa (e.g., anther open-ing by valves, spiral fl oral phyllotaxis, inner staminodes, trim-erous fl owers), it was possible to entertain several alternative models for the ancestral fl ower (e.g., Endress, 1986a ). However, especially since 1999, a more precise discussion is possible be-cause phylogenetic reconstructions are generally more advanced, and specifi cally the topology of the basal grade of extant angio-sperms is well supported and can be used as a basis for discus-sions on evolution. As emphasized by Crisp and Cook (2005) , it cannot be assumed that single low-diversity “ basal ” lines are plesiomorphic in any given character, but when several lines branch sequentially below the vast bulk of a clade, as is appar-ently the case for angiosperms, and these lines share the same character state, this state can be reconstructed by parsimony analysis as ancestral. We took advantage of the new evidence on rooting in an analysis of basal angiosperms (including basal monocots and basal eudicots), in which we used parsimony op-timization on a tree based on morphological data and rbcL , atpB , and 18S rDNA sequences ( Soltis et al., 2000 ) to estimate ancestral states and trace character evolution ( Doyle and Endress, 2000 ). In later articles we concentrated on implica-tions of this data set for evolution of pollen morphology ( Doyle, 2005 ), leaf architecture ( Doyle, 2007 ), fl oral phyllotaxis ( Endress and Doyle, 2007 ), and the position of Hydatellaceae ( Saarela et al., 2007 ). This “ angiosperm-centered ” or “ top-down ” approach ( Bateman et al., 2006 ) can be questioned on the grounds that in theory outgroup and ingroup relationships cannot be addressed separately. However, in practice this seems less problematical than anticipated, thanks to the increasingly robust rooting of angiosperms based on molecular data.

In the present paper we discuss changes in our perception of the fl ower in the most recent common ancestor of living angio-sperms (the crown group node) and its initial evolutionary mod-ifi cations, using an updated version of the Doyle and Endress (2000) data set and taking into account new evidence from phy-logenetic and structural studies on extant plants, fossils, and evo-devo studies. It is unlikely that this “ ancestral fl ower ” was the “ fi rst fl ower ” in a morphological sense, which may have originated much earlier on the angiosperm stem lineage. We will not consider the origin of the angiosperm fl ower in relation to reproductive structures in outgroups, which requires consid-eration of fossil seed plants, a topic treated elsewhere ( Doyle, 2006 , 2008).

Our previous study ( Doyle and Endress, 2000 ) presented a list of inferred ancestral states for all characters, but this needs reassessment in light of new data. Since 2000, we have been revising our data set by adding new characters, refi ning old ones, adding new taxa, and splitting taxa into more homogeneous units to analyze character evolution in more detail and fi ll in less well sampled parts of the tree. We have not yet performed a new combined analysis of morphological and molecular data, but we have made changes in the tree used as a framework for discussion where recent data provide robust evidence for differ-ent relationships. For example, our previous combined analysis linked Piperales with monocots, but accumulating molecular data ( Zanis et al., 2002 ; Sauquet et al., 2003 ; Qiu et al., 2005 , 2006 ) consistently associate them with Canellales (Canellaceae, Win-teraceae), Magnoliales, and Laurales, in a clade named Magnolii-dae by Cantino et al. (2007) , not to be confused with Magnoliidae in the paraphyletic sense of Takhtajan (1964) and others.

All other angiosperms form a strongly supported clade, named Mesangiospermae by Cantino et al. (2007) , but relationships among several lines in this clade remain poorly resolved, prob-ably as a result of very rapid radiation ( Moore et al., 2007 ). One important area of current uncertainty is the position of Chloran-thaceae, which have been the subject of much discussion be-cause of their extremely simple fl owers. Combined analyses of morphological and molecular data ( Doyle and Endress, 2000 ) and some molecular studies ( Qiu et al., 2005 ; Duvall et al., 2006 ; Mathews, 2006 ) have placed Chloranthaceae at the base of mesangiosperms, but they are nested within mesangiosperms in most molecular trees, including most of those found in analy-ses of complete plastid genomes ( Jansen et al., 2007 ; Moore et al., 2007 ). Suggestions that fl owers of Chloranthaceae were primitive based on the abundance of apparently related fossils in the Early Cretaceous (reviewed by Eklund et al., 2004 ; Friis et al., 2006 ) have faded with fi rm establishment of the basal ANITA grade, but if Chloranthaceae are sister to the remaining mesangiosperms they could still be relevant to reconstruction of the original fl ower and its initial modifi cations.

Comparative studies of fl oral developmental genetics repre-sent another growing fi eld that promises to provide new insights on early fl oral evolution. Such studies have already been used for interpolations between angiosperms and other living seed plants and within angiosperms ( Frohlich and Parker, 2000 ; Frohlich, 2003 , 2006 ; Baum and Hileman, 2006 ; Irish, 2006 ; Soltis et al., 2006 ; Frohlich and Chase, 2007 ; Theissen and Melzer, 2007 ).

Several spectacular new fi ndings have brought the aquatic habitat to the center of the attention and debate on early angio-sperm evolution (e.g., Sun et al., 2002 ; Friis et al., 2003 ; Crepet et al., 2004 ; Feild and Arens, 2007 ). These are (1) the recogni-tion of new aquatic angiosperms in the Early Cretaceous fossil record, including Archaefructus ( Sun et al., 1998 , 2002 ; Friis et al., 2003 ; Ji et al., 2004 ), which had fertile axes bearing paired stamens, single or paired carpels, and no perianth; Monsechia , tentatively interpreted as a bryophyte when it was fi rst described ( Gomez et al., 2006 ); and Scutifolium , assigned to Cabom-baceae ( Taylor et al., 2008 ), in addition to previously recog-nized water plants such as Nelumbites ( Doyle and Hickey, 1976 ; Upchurch et al., 1994 ; Mohr and Friis, 2000 ; Wang and Dilcher, 2006 ); (2) the discovery that the submerged water plant family Hydatellaceae belongs not in monocots but rather to Nymphaeales in the ANITA grade ( Saarela et al., 2007 ); and (3) indications from some (though not most) molecular analy-ses that the aquatic genus Ceratophyllum (= Ceratophyllaceae), which had a brief period of fame as the inferred sister group of all other angiosperms in analyses of rbcL ( Chase et al., 1993 ), may belong just above the basal angiosperm grade, with Chlo-ranthaceae ( Duvall et al., 2006 ; Mathews, 2006 ; Qiu et al., 2006 ). The importance of fresh-water habitats and fl ood plains in early angiosperm history has long been recognized by paleo-botanists ( Doyle and Hickey, 1976 ; Taylor and Hickey, 1992 ), and continues to be a major topic of discussion by paleoecolo-gists ( Mart í n-Closas , 2003 ; Feild et al., 2004 ; Coiffard et al., 2007 ; Feild and Arens, 2007 ). The impression that Early Creta-ceous angiosperms included a large number of water plants may be partly due to a bias in favor of fossilization of aquatics over other plants, but water plants were clearly more common than expected under the old view that the initial diversifi cation of angiosperms involved woody plants (cf. Doyle and Hickey, 1976 ).

Until about ten years ago, only a vague recognition of more widespread features in basal angiosperms was possible. They

24 American Journal of Botany [Vol. 96

phylogenetic analyses, particularly those related to rooting, to estimate ances-tral states. Our assumptions on rooting of taxa and the publications on which they are based are cited in the taxon list. Improved information on relationships within taxa has led us to make many minor changes in scoring of taxa since Doyle and Endress (2000) .

Taxa — Besides adding Ceratophyllum and Hydatellaceae, we have in-creased our taxon sampling in other groups. In Chloranthaceae, we split Chlo-ranthus and Sarcandra , treated as one taxon in Doyle and Endress (2000) , into the two genera and rescored several characters based on Eklund et al. (2004) . In Ranunculales, we have added Circaeaster and split Hydrastis and Glaucidium from “ core ” Ranunculaceae (their sister group according to Hoot et al., 1999 ) because they differ substantially in fl oral features and may thus affect recon-struction of fl oral evolution. For the same reason, we split Magnoliaceae into Liriodendron and Magnolioideae ( Magnolia s. l. of recent authors) and Trocho-dendraceae into Trochodendron and Tetracentron . We have modifi ed the scor-ing of Platanaceae (now Platanus ) and Buxaceae, in which we previously included presumed fossil relatives, to apply strictly to the extant crown groups, in anticipation of testing the position of the fossils. We have increased our sam-pling of Alismatales for future tests of comparisons with fossils. We have added Nartheciaceae because they appear to be related to but less modifi ed than Di-oscoreaceae ( Caddick et al., 2002a ), and Melanthiaceae as a relatively ple-siomorphic exemplar of Liliales ( Chase et al., 2006 ).

In Ceratophyllum , the fertile structures have been variously interpreted ( Endress, 1994b ; Iwamoto et al., 2003 ): at one extreme, as female fl owers with a single carpel surrounded by tepals and as male fl owers with tepals and numer-ous stamens; at the other, as female fl owers with no perianth but bracts lower on the axis and as spikes with basal bracts and numerous male fl owers consist-ing of one stamen, with no perianth or individual subtending bract ( Endress, 2004 ). For the purposes of this analysis, we have provisionally accepted the second interpretation. First, in the female structures, single carpels occasionally occur in the axils of the sterile appendages ( Aboy, 1936 ; Iwamoto et al., 2003 ), suggesting that the latter are bracts rather than tepals and the system is a re-duced infl orescence. Second, the stamens have an extremely labile phyllotaxis and marked acropetal delay in maturation ( Endress, 1994b ), which is a common pattern in fl owers of spicate infl orescences but anomalous within the androe-cium of a multistaminate fl ower.

Our scoring of Archaefructus is based on whole plants of A. liaoningensis and A. sinensis ( Sun et al., 1998 , 2001 , 2002 ; Friis et al., 2003 ); features are generally consistent in A. eofl ora ( Ji et al., 2004 ), which may represent either a smaller species or a younger stage of A. sinensis . We analyzed the position of Archaefructus using two alternative scorings, one ( Archaefructus inf) assuming that fertile axis was a raceme of male and female fl owers consisting of usually two stamens and one or two carpels, the other ( Archaefructus fl o), following Sun et al. (2002) , that it was a bisexual fl ower or prefl ower with paired stamens be-low and carpels above. Friis et al. (2003) questioned whether the bodies that Sun et al. (2001 , 2002 ) described as pollen were in fact pollen grains, because of their irregular size and shape, but we provisionally assume that at least some of them are pollen and have scored them based on the most convincing specimen, illus-trated in Fig. 2F of Sun et al. (2002) . To evaluate the alternative interpretation, we have used a third scoring ( Archaefructus NP) that corresponds to Archaefructus inf with pollen characters treated as unknown. Sun et al. (1998 , 2002 ) described the carpels as conduplicate (= plicate), but in extant carpels of similar appear-ance this cannot be determined without developmental or anatomical evidence ( Friis et al., 2003 ; Endress, 2005 ). They described the fruits as follicles, but they did not actually report dehiscence. The seeds appear to have a palisade exotesta as defi ned here (character 101, including not only radially elongated but also shorter sclerotic cells): Sun et al. (1998 , 2002 ) described the surface as consist-ing of epidermal cells with cutinized anticlinal and periclinal walls.

Ji et al. (2004) interpreted seeds of A. eofl ora as orthotropous, but their pub-lished illustrations are not clear enough to determine whether the seeds were anatropous or orthotropous; the fi gure of the end of a seed in Fig. 2C of Sun et al. (1998) is actually more suggestive of an anatropous ovule. Hence we have scored ovule curvature (93) as unknown. Ji et al. (2004) described one lateral unit in A. eofl ora as bisexual, with one stamen and two carpels, and they also interpreted one unit in the type specimen of A. sinensis ( Sun et al., 2002 ) as bisexual. Under our character defi nition, A. eofl ora might be scored as uncertain (0/1) for fl ower sexuality (26). However, we believe it would be premature to rescore Archaefructus as a whole in this way.

Characters — In this study we have not included all the characters in our most recent version of the Doyle and Endress (2000) data set, many of which are not relevant for our present purposes, where we have used fi xed backbone

Our most important change in taxon sampling is the addition of two aquatic groups: Hydatellaceae, now linked with Nympha-eales ( Saarela et al., 2007 ), and Ceratophyllum . In Doyle and Endress (2000), we omitted Ceratophyllum because many char-acters in our matrix were lacking or uninterpretable due to re-duction, its position was unstable in preliminary analyses, and we assumed it would have a minor effect on inferences on char-acter evolution because of its specialized, reduced nature. How-ever, omitting Ceratophyllum is no longer justifi able in light of the increasing number of other near-basal taxa with simple fl owers and the suggestion that they represent a prefl oral state ( Friis and Crane, 2007 ). Whether such fl owers are reduced should be tested rather than assumed. The claim that Cerato-phyllum is the sister group of eudicots, based on analyses of complete plastid genomes ( Jansen et al., 2007 ; Moore et al., 2007 ), also needs to be evaluated in light of morphological data and its implications explored.

Another major change is addition of the Early Cretaceous fossil plant Archaefructus , which a cladistic analysis by Sun et al. (2002) identifi ed as the sister group of all extant angio-sperms (i.e., a stem relative). This interpretation was questioned by Friis et al. (2003) , who interpreted Archaefructus as a crown group angiosperm with reduced unisexual fl owers, but reaffi rmed by Crepet et al. (2004) . In either case, its unusual combination of characters make it potentially relevant to reconstruction of the ancestral fl ower. The addition of Archaefructus is part of a general effort to integrate fossils into the phylogeny of living basal angiosperms ( Doyle and Endress, 2007 ). Results of our analyses concerning other fossil taxa are not presented here be-cause they have less impact on reconstruction of the ancestral fl ower. Some of these fossils are too deeply nested within mag-noliids and eudicots to affect inferred ancestral states; others may be more basal (e.g., taxa apparently related to Chloran-thaceae: Eklund et al. [2004]) but add few new elements be-cause they resemble their presumed extant relatives in fl oral features.

Besides considering implications of current phylogenies for evolution of individual fl oral characters and character com-plexes, we stress several specifi c broader issues. These include (1) what present data say about evolutionary interpretation of the fl owers of Magnoliales and Winteraceae, once widely as-sumed to be primitive; (2) whether the simple fl ower structure in some basal angiosperms (Hydatellaceae, Archaefructus , Cer-atophyllum , Chloranthaceae) is due to reduction of more “ com-plete ” fl owers, retention of a “ prefl oral ” state, or to breakdown of the distinction between fl owers and infl orescences due to loss of fl oral identity, issues raised by Friis and Crane (2007) and Rudall et al. (2007) , and if and how this might be related to an aquatic habit; and (3) what the evolutionary consequences of a position of Chloranthaceae just above the basal grade, with or without Ceratophyllum ( Doyle and Endress, 2000 ; Duvall et al., 2006 ; Mathews, 2006 ; Qiu et al., 2006 ), would be for in-terpretation of the fl owers in these groups, and how these would differ in the context of the plastid genome trees ( Jansen et al., 2007 ; Moore et al., 2007 ), where the two taxa are nested sepa-rately within mesangiosperms.

MATERIALS AND METHODS

Lists of taxa and characters and the data matrix are presented in Appendix 1. In dealing with characters that vary within taxa, we have not simply scored characters as uncertain ( “ polymorphic ” ) but have made use of results of


Scoring the number of perianth and stamen whorls (34, 43) is straightfor-ward in whorled taxa (except for seemingly tetramerous fl owers that actually have dimerous whorls, as in Proteaceae, Tetracentron , and Buxaceae, as in-ferred from the fact that the stamens appear to be opposite the tepals: von Balt-hazar and Endress, 2002a; Chen et al., 2007 ), but again the treatment of spiral taxa poses problems. Many spiral taxa (and Nelumbo , with chaotic stamen in-sertion on an androecial ring meristem: Hayes et al., 2000 ) have numbers of tepals and/or stamens that are comparable to those of taxa with more than two whorls, so we have scored them accordingly. We also used the number of series (in which a certain number of parts fi lls the circumference of the fl ower; En-dress and Doyle, 2007 ) as a rough substitute for number of whorls.

In most basal angiosperms, all perianth parts are best described as tepals ( Hiepko, 1965 ; Walker and Walker, 1984 ; Endress, 2001 ; Ronse De Craene, 2008 ) because they are less strongly differentiated than the typical sepals and petals of core eudicots ( Pentapetalae of Cantino et al., 2007 ). These tepals may be uniform (either sepaloid or petaloid) or differentiated into outer sepaloid and inner petaloid parts, distinctions recognized in character 35. We include both tepals and more differentiated petals in the count of whorls, and staminodes as well as fertile stamens. However, we also introduced a separate character (36) for presence or absence of typical petals (mostly in Ranunculales), defi ned on more pronounced differences in anatomy and delay in development. Taxa with petals may show differentiation within the outer perianth whorls, such as Nuphar , which has outer sepaloid and inner petaloid “ tepals ” or “ sepals ” and much smaller petals.

We have made fewer changes from Doyle and Endress (2000) in characters of individual fl oral parts. Following Eklund et al. (2004) , to reduce uncertain scorings, we modifi ed the stamen base character (48) to combine short and wide and short and narrow in the same state, and the orientation character (53) to combine slightly introrse with latrorse. We previously treated modes of carpel sealing as a multistate character (corresponding to the four types of Endress and Igersheim, 2000a ). However, carpel sealing has two potentially independent aspects, degree of postgenital fusion and secretion, which we have split into two characters (76, 77). We separated types of papillae (82) from larger protu-berances (81), because pluricellular papillae and protuberances co-occur in Am-borella and Trimenia but not in other taxa and therefore appear to represent independent characters.

Many aspects of fl oral evolution were also treated by Ronse De Craene et al. (2003) . They made less effort to ensure independence of characters: for exam-ple, lack of perianth was a state in three of their characters. This was not neces-sarily a problem in their study, in which they plotted characters on a molecular tree, and it may be useful in assessing the implications of different character defi nitions. However, such redundancy poses problems if characters are used for tree reconstruction, since it may overweight what was presumably a single change — for example, loss of perianth. Because we intend to use our data set in a future combined analysis and have used it to investigate the relationships of Ceratophyllum and Archaefructus in the current study, we have tried to mini-mize redundancy among characters.

Infl orescence characters deserve special attention as an area where we have made major modifi cations. In our previous analysis ( Doyle and Endress, 2000 ), we recognized a relatively crude infl orescence character emphasizing degree of branching, with three states: solitary fl owers; racemes, spikes, and botryoids; and more richly branched infl orescences such as panicles and compound infl o-rescences of racemes, spikes, and botryoids. Thus in infl orescences of the sec-ond state, we did not recognize the standard contrast between indeterminate and determinate infl orescences, or the related distinction of Troll (1964) and We-berling (1989) between polytelic systems with no terminal fl ower (racemes, spikes, thyrses) and monotelic systems in which all axes terminate with a fl ower (botryoids, thyrsoids, panicles — all sometimes imprecisely described as “ cymes ” ). This was because of a perception that the two types intergrade within taxa, such that many taxa would have to be scored as uncertain. However, closer examination has led us to conclude that a different grouping of traditional types into basically monotelic and polytelic states (in character 22, Fig. 1 ) leads to fewer problems than we had thought and is more informative: one state in-cludes units lacking a terminal fl ower (racemes, spikes, thyrses), the other those with a terminal fl ower (botryoids, thyrsoids, panicles). Although taxa often vary between types within each of these states, there is less variation between types belonging to the different states.

Racemes and thyrses differ on whether the lateral units on the indeterminate axis are single fl owers or cymes. Cymes are branching systems that can have one to several branching orders (i.e., a main axis and lateral branches of one to several orders formed by repeated branching of these laterals), but each axis has not more than two lateral branches of the next higher order, and all axes are usually determinate. Botryoids are the other way around: they have only one

constraint trees as a framework for placement of Ceratophyllum and Archae-fructus and reconstruction of fl oral evolution, and would require excessively lengthy documentation and argumentation. We have included all fl oral charac-ters, including those of stamen, carpel, and ovule morphology. In addition, we include all those nonfl oral characters needed for analysis of the position of Cer-atophyllum and Archaefructus . Characters omitted because they do not exist or are inapplicable in Ceratophyllum include aspects of secondary xylem and phloem, leaf anatomy, and the inner and outer integuments, which are reduced or fused into a single integument.

Some of the most important and complex arguments for decisions in defi ni-tion of characters and scoring of particular taxa are discussed in this section, others that are less problematic or signifi cant in Appendix 1. Because of space limitations, we cite only general sources of information for particular character sets and especially important references on particular taxa, and reserve more detailed documentation and resolution of differences between our interpreta-tions and those of other workers for elsewhere. We concentrate on references for new taxa and characters; for those used in Doyle and Endress (2000) , read-ers are referred to that article.

Our general philosophy on defi nition of characters is explained in more de-tail in Doyle and Endress (2000) . Few of our characters are quantitative in the sense of continuous (e.g., pollen size, nexine thickness), but there are often se-ries of conditions that could be grouped into many states or a few. In general, we have tried to break the variation into a smaller number of states in ways that make morphological (especially developmental) sense and reduce the number of uncertain ( “ polymorphic ” ) scorings of taxa (assuming that this reduction is evidence that the variations included in each of the states are related). Several important changes concern replacement of multistate with binary characters, which can sometimes improve resolution of relationships in cases where the optimization of a multistate character would be ambiguous. In several cases we previously used unordered multistate characters to combat the Maddison “ long distance ” effect ( Maddison, 1993 ): where the ancestral state in one clade in which a structure (more generally a character) occurs in two (or more) versions infl uences the polarity of the character in another clade that has the structure, even though the structure does not exist in the intervening lines and presumably arose independently. This artifact can be avoided by treating lack of the struc-ture as one state of a multistate character and different versions of the structure as other states. However, this procedure weakens the contrast between presence and absence of the structure as an independent source of information on relationships.

An example that underlines the importance of the Maddison effect concerns presence or absence of a perianth. In Doyle and Endress (2000), we treated the number of perianth whorls as an unordered multistate character, with no peri-anth one of four states. A group where this may cause problems is Chloran-thaceae, where Hedyosmum has one perianth whorl and the other genera have no perianth. Since most outgroups have a perianth, its presence might appear to be evidence for the basal position of Hedyosmum , or in other words its loss could be evidence for the monophyly of the remaining genera (which is sup-ported by molecular evidence). However, when presence and number of whorls are treated as a single unordered multistate character, scoring Hedyosmum as having one whorl does not favor a basal position in Chloranthaceae because the outgroups have two or more whorls, states that are not recognized as any more similar to one whorl than to none. For this reason, Eklund et al. (2004) split the Doyle and Endress (2000) character into two — one for presence or absence of a perianth, the other for number of whorls, with taxa lacking a perianth scored as unknown — and we have followed this solution here (characters 31, 34). Maddison (1993) pointed out cases where this procedure is unlikely to cause problems, notably where loss of a structure occurs in a terminal clade. With relationships largely inferred from molecular data, cases where this may cause artifacts can usually be recognized and treated in discussion.

Additional important changes involve other characters of fl oral organization. In Doyle and Endress (2000), we recognized phyllotaxis and merism (merosity) as separate characters in both the perianth and the androecium, but this poses problems for scoring of merism in spiral taxa. Our solution was to treat merism as a multistate character, with spiral taxa scored as (0) irregular and whorled taxa as (1) trimerous or (2) dimerous, tetramerous, or pentamerous. However, this may introduce bias due to redundancy of spiral phyllotaxis and irregular merism. One solution would be to combine phyllotaxis and merism into a single character, but as discussed in Endress and Doyle (2007) , the distinction between spiral and whorled appears to be consistent and independent enough to be treated separately. Our solution is to retain both characters (32, 33 for the peri-anth; 41, 42 for the androecium) but score spiral taxa as unknown for merism. Optimization of this character across the tree produces artifactual reconstruc-tions of merism in spiral taxa, but this can be considered in discussion.


state (in character 22, Fig. 1 ): there is variation between these two extremes in many taxa, such as Austrobaileya , Eupomatia , Magnoliaceae, and Calycan-thaceae. If the axillary branch (pedicel) bearing the fl ower has no appendages or at most one or two prophylls, we call the system a raceme; if it has more sterile appendages, we call the fl ower solitary. This defi nition allows most taxa to be scored unambiguously. Schisandraceae are still mixed (0/1), since the number of bracteoles varies between zero and three or more among species ( Weberling, 1988 ; Saunders, 2000 ). Special problems in interpretation of Nymphaeales are treated in the Discussion, since they make more sense in a phylogenetic context.

When fl owers are unisexual and the infl orescences of male and female fl ow-ers differ in type, we have scored the taxon based on the more complex type. Thus, we have scored Hedyosmum , with male spikes and female thyrses, as having thyrses; and Ceratophyllum , with solitary female fl owers and male spikes, as having spikes.

Except for three pollen characters (see Appendix 1), all multistate characters were treated as unordered.

Analyses — Our analyses (all based on parsimony) used “ backbone con-straint ” trees, with Recent taxa fi xed into one of two topologies. Analyses were performed with the program PAUP* version 3.1.1 ( Swofford, 1990 ) and in-volved 10 or 100 heuristic replicates, stepwise random addition of taxa, and tree-bisection-reconnection (TBR) branch swapping. The relative parsimony of alternative relationships was determined by searching for trees less than or equal to a given number of steps and observing the trees obtained or by moving taxa manually with MacClade ( Maddison and Maddison, 2003 ).

The fi rst backbone tree (henceforth labeled D & E) is a modifi cation of the tree found in our morphological and three-gene analysis ( Doyle and Endress, 2000 ), with changes where accumulating molecular data have most strongly and consistently contradicted relationships found in our previous study. Essen-tially this is a handmade supertree. Besides linking Piperales with Canellales, as already discussed, we have moved Euptelea from within Ranunculales to the base of the order, following Kim et al. (2004a) ; this position is actually more parsimonious in terms of morphology. Taxa added or split for the reasons dis-cussed earlier have been placed following Les et al. (1997) , Hoot et al. (1999) , Soltis et al. (2000) , Chen et al. (2004) , and Chase et al. (2006) . In a preliminary analysis, we added Ceratophyllum to the data set and constrained all other rela-tionships as described. The tree found in this constrained analysis is the modi-fi ed D & E backbone tree used in subsequent analyses.

The second backbone tree (labeled J/M) incorporates relationships of major clades found in analyses of whole plastid genomes by Jansen et al. (2007) and Moore et al. (2007) , notably with Chloranthaceae linked with magnoliids, Cer-atophyllum with eudicots, and the latter two with monocots. The same relation-ships were found by Saarela et al. (2007) in analyses of a smaller plastid data set. Relationships within clades (which were sparsely sampled in the plastid studies) are the same as in the D & E backbone tree.

To investigate the position of Archaefructus , we analyzed the data set with Archaefructus added, using both backbone trees. To assess implications of the hypothesis that Amborella and Nymphaeales form a clade, we rerooted trees manually with the program MacClade version 4.03 ( Maddison and Maddison, 2003 ).

We used MacClade to optimize character evolution on trees, reconstruct ancestral states, and identify characters supporting relationships. When we re-fer to features as unequivocal synapomorphies of particular clades, this does not mean they are uniquely derived, but rather that the change in state unequivo-cally occurs at this point on the tree, as opposed to cases where the position of change is equivocal (e.g., where an earlier origin followed by a reversal and two later origins are equally parsimonious, or where the character state in neighbor-ing taxa is unknown).

RESULTS

When Ceratophyllum is added to the updated Doyle and En-dress (2000) tree, its most parsimonious position is as the sister group of Chloranthaceae (776 steps; Fig. 2A ). It is nested within Chloranthaceae in all six trees that are one to three steps longer. A position as the sister group of eudicots ( Jansen et al., 2007 ; Moore et al., 2007 ) is nine steps less parsimonious (785 steps); a position as the sister group of monocots is eight steps less parsimonious (784 steps).

branching order (i.e., a main branch and lateral branches of only the fi rst order), but the number of fi rst-order lateral branches is not limited until the terminal fl ower is formed; as in cymes the axes are determinate. When there is only one branching order and axes have only one or two lateral fl owers, cymes and botryoids cannot be distinguished unless more highly branched units are found. Racemes and thyrses both occur within taxa such as Chloranthaceae, where Hedyosmum has thyrses of female fl owers and spikes of male fl owers, and some species of Ascarina have spikes, others thyrses. We have recognized this dis-tinction with a separate character (23, lateral units single fl owers or cymes). We have also distinguished racemes from spikes by introducing a character con-trasting pedicellate and sessile fl owers (24).

Another important distinction concerns the presence or absence of bracts or leaves (pherophylls) subtending the fl owers (25). In Archaefructus , Sun et al. (2002) cited the absence of bracts below the paired stamens and carpels as evi-dence that the fertile axis was a fl ower (or prefl ower) rather than an infl ores-cence. However, subtending bracts are absent in several groups in the present data set, such as Hydatellaceae, Acorus , and Araceae.

Other problems concern the distinction between solitary fl owers and ra-cemes, specifi cally when solitary fl owers are borne in the axils of more or less unmodifi ed vegetative leaves. Solitary axillary fl owers are sometimes distin-guished from lateral fl owers in a raceme based on whether they are subtended by normal leaves or modifi ed bracts, but this is more a matter of degree than a fundamental difference in organization. This problem is illustrated by cases in which fl owers are borne in the axils of bracts on an axis that then reverts to producing vegetative leaves (e.g., Schisandra , Euptelea ; Endress, 1969 ; We-berling, 1988 ). In our previous analysis we scored these as solitary. Alterna-tively, even systems with fl owers in the axils of normal leaves are sometimes described as racemes ( Weberling, 1989 ). Because mode of branching seems more fundamental than variation between bracts and leaves, we have adopted this approach, grouping systems where fl owers are borne in the axils of bracts and regular leaves as racemes. We group fl owers that terminate either a long shoot (the classic terminal condition) or an axillary short shoot in the solitary

Fig. 1. Sketches illustrating infl orescence types included in three states of infl orescence character (22). (A, B) = state 0; (C – E) = state 1; (F – H) = state 2. (A) solitary, terminal; (B) solitary, axillary; (C) botryoid; (D) panicle; (E) thyrsoid; (F, G) raceme; (H) thyrse.


Fig. 2. Representative most parsimonious trees obtained after addition of Archaefructus to backbone constraint trees of Recent basal angiosperms. OM and OE indicate presumed positions of other monocots and other eudicots, respectively. (A) Using D & E backbone tree, from combined morphological and molecular analysis of Doyle and Endress (2000) , with modifi cations based on more recent data. (B) Using J/M backbone tree, with relationships among major clades found in plastid genome analyses of Jansen et al. (2007) and Moore et al. (2007) , but with relationships within clades as in Fig. 2A . Nymph = Nymphaeales, Aust = Austrobaileyales, Chlor = Chloranthaceae, Piper = Piperales, Ca = Canellales, Magnol = Magnoliales.


When Archaefructus is scored as having an infl orescence of unisexual fl owers ( Archaefructus inf) and added to the D & E backbone tree, its single most parsimonious position is as the sister group of Hydatellaceae (782 steps; Fig. 2A ). Its next best position (one step worse) is sister to the remaining Nymphae-ales (henceforth designated “ core Nymphaeales ” ). Seven posi-tions are two steps worse: sister to all Nymphaeales, Cabomba , Ceratophyllum , the Chloranthaceae- Ceratophyllum clade, all mesangiosperms except the Chloranthaceae- Ceratophyllum clade, and either Euptelea or Circaeaster in the eudicots.

The J/M backbone tree based on plastid genome data ( Jansen et al., 2007 ; Moore et al., 2007 ) is 10 steps longer than the D & E tree (786 steps). When Archaefructus (inf) is added to the J/M backbone tree, its most parsimonious position is sister to Cer-atophyllum (791 steps; Fig. 2B ). Next best are positions linked with Hydatellaceae (one step worse) and sister to core Nympha-eales (two steps worse).

If pollen characters of Archaefructus are scored as unknown ( Archaefructus NP), its most parsimonious position with the D & E backbone (781 steps; not shown) is sister to the eudicot genus Euptelea (Ranunculales). Its next most parsimonious posi-tions (782 steps) are sister to Hydatellaceae, Ceratophyllum , Cer-atophyllum plus Chloranthaceae, Ranunculales other than Euptelea , Circaeaster (also Ranunculales), and the clade consist-ing of eudicots, monocots, and magnoliids. With the J/M back-bone, omitting pollen characters strengthens the association of Archaefructus with Ceratophyllum (789 steps), which becomes three steps rather than one step more parsimonious than its next-best positions (792 steps), which are sister to Hydatellaceae, Euptelea , Ranunculales other than Euptelea , and Circaeaster .

When Archaefructus is scored as having a bisexual fl ower ( Archaefructus fl o) and added to the D & E backbone tree, it has three most parsimonious positions (783 steps; not shown): sis-ter to Hydatellaceae, Cabomba , and core Nymphaeales. Seven positions are one step worse, including not only elsewhere in Nymphaeales but also sister to Magnoliales plus Laurales, Magnoliaceae, Circaeaster plus Lardizabalaceae, and Cir-caeaster . When it is added to the J/M backbone tree, it has four most parsimonious positions (793 steps), including those found with the D & E backbone and as the sister group of Ceratophyllum .

Characters supporting these relationships of Ceratophyllum and Archaefructus are presented in the Discussion section. A list of inferred ancestral states in angiosperms for fl oral charac-ters is presented in Table 1 , with differences among eight trees, involving all combinations of the D & E vs. J/M backbone trees, Amborella sister to all other angiosperms vs. Amborella and Nymphaeales forming a clade, and exclusion vs. inclusion of Archaefructus . Parsimony optimizations of selected characters on various trees are presented in Figs. 3 – 12 .

D ISCUSSION

Phylogenetic results — Our inference that Ceratophyllum is related to Chloranthaceae is supported by fi ve unequivocal sy-napomorphies: sessile fl ower (character 24), one stamen (40), embedded pollen sacs (51), one carpel (74), and orthotropous ovule (93). Synapomorphies of Chloranthaceae that are not found in Ceratophyllum and thereby place Ceratophyllum out-side the family are sheathing leaf bases (12), interpetiolar stipules (13), and stigmatic protuberances (81). Remarkably, it is only one step less parsimonious to nest Ceratophyllum within Chloranthaceae, where its best position is sister to Hedyosmum ,

supported by loss of bracts subtending the male fl owers (25) and dry fruit wall (97).

A sister group relationship of Ceratophyllum and eudicots, as found in the plastid genome analyses of Jansen et al. (2007) and Moore et al. (2007) and many other molecular analyses (e.g., Saarela et al., 2007 ), is nine steps less parsimonious and would be supported by only one unequivocal morphological synapo-morphy, dry fruit wall (97), a highly homoplastic character. It is eight steps less parsimonious to link Ceratophyllum with mono-cots, which would be supported by loss of cambium (4). Whether this parsimony differential is suffi cient to overrule the molecular support for a relationship with eudicots needs to be tested by future combined analyses. However, it should be noted that bootstrap support for the link between Ceratophyl-lum and eudicots is only modest (71% in Moore et al., 2007 ; 74 – 89% in Saarela et al., 2007 ); that analyses by Moore et al. (2007) using various methods and subsets of data gave different topologies, some with Chloranthaceae in a more basal position; and that other molecular analyses have linked Ceratophyllum with Chloranthaceae ( Duvall et al., 2006 ; Mathews, 2006 ; Qiu et al., 2006 ). The strength of the morphological synapomor-phies might be questioned on the grounds that they largely rep-resent reductions and simplifi cations from ancestral states in angiosperms, which might be expected to give similar results regardless of their starting point. However, this is not in itself evidence that they are systematically worthless: without Cer-atophyllum all these features are valid synapomorphies of Chlo-ranthaceae, which are independently supported as a clade by molecular data.

These results suggest the intriguing possibility that Cerato-phyllum is an aquatic derivative of a terrestrial stem relative of Chloranthaceae that already had many features of the crown group. Many additional changes would have to occur on the line leading to Ceratophyllum : origin of a protoxylem lacuna (2), loss of cambium (4), loss of pericyclic fi bers (6), dissection of the leaves (20) and shift to dichotomous venation (18), loss of pollen aperture (62) (and almost total reduction of the exine: Takahashi, 1995 ), loss of stigmatic papillae (82), reduction or fusion of the integuments to one (94), and large embryo (109). Chloranthaceae and their extinct relatives are emerging as one of the fi rst successful angiosperm lines ( Eklund et al., 2004 ; Feild et al., 2004 ), which included greater diversity than would be inferred from the four living genera alone. Our results con-cerning Ceratophyllum therefore raise the possibility that some Early Cretaceous carpels or pollen that resemble Chloran-thaceae might actually be closer to Ceratophyllum and might therefore provide evidence on steps in its origin.

Our analysis provides provisional support for the speculative suggestion of Saarela et al. (2007) that Archaefructus is related to Hydatellaceae. This is the most parsimonious position of Archae-fructus when its fertile axis is interpreted as a raceme of unisexual fl owers and Ceratophyllum is associated with Chloranthaceae, as with the D & E backbone. Unequivocal synapomorphies of the two groups are loss of fl oral subtending bracts (25) and loss of perianth (31). The fact that the fl owers are unisexual is consistent but not indicative because the polarity of this character is equivo-cal. Other features of Archaefructus that support a relationship to Nymphaeales as a whole are palmate venation (17) (reduced to one vein in Hydatellaceae), boat-shaped pollen (61), and palisade exotesta (101). This result would suggest that Hydatellaceae may be what became of one member of the Archaefructus group after 125 Myr of further reduction in an aquatic habitat.


D&E J/M

A,N R A+N R A,N F A+N F A,N R A+N R A,N F A+N F

22. Infl orescence 0 solitary, 1 botryoid etc., 2 raceme etc. 1/2 2 1/2 2 1/2 2 1/2 223. Infl orescence units 0 single fl ower, 1 cymes 0 solitary fl ower24. Pedicel 0 present, 1 absent (sessile) 0 present25. Bracts 0 present, 1 absent in male, 2 absent in all 0 present26. Sex of fl owers 0 bisexual, 1 unisexual 0/1 bi/unisexual27. Hypanthium 0 absent, 1 present, 2 inferior ovary 0/1 0 0/1 0 0/1 0 0/1 028. Receptacle 0 short, 1 elongate 0 short29. Cortical vasculature 0 none or P, 1 A, 2 A plus G 0 none30. Floral apex 0 used up, 1 protruding 0 used up31. Perianth 0 present, 1 absent 0 present32. Perianth phyllotaxis 0 spiral, 1 whorled 0/1 spiral/whorled33. Perianth merism 0 trimerous, 1 dimerous, 2 polymerous 0 trimerous34. Perianth whorls 0 one, 1 two, 2 more than two 2 more than two35. Tepal differentiation 0 sepaloid, 1 sep + pet, 2 petaloid 0/1 1 0/1 1 0/1 1 0/1 136. Petals 0 absent, 1 present 0 absent37. Inner perianth nectaries 0 absent, 1 present 0 absent38. Outer perianth fusion 0 free, 1 fused 0/1 0 0/1 0 0/1 0 0/1 039. Calyptra 0 absent, 1 present 0 absent40. Stamen number 0 more than one, 1 one 0 more than one41. Stamen phyllotaxis 0 spiral, 1 whorled 0/1 spiral/whorled42. Stamen merism 0 trimerous, 1 dimerous, 2 polymerous 0 trimerous43. Stamen whorls 0 one, 1 two, 2 more than two 2 more than two44. Stamen position 0 single, 1 double 0 single45. Stamen fusion 0 free, 1 connate 0 free46. Inner staminodes 0 absent, 1 present 0 absent47. Food bodies 0 absent, 1 on staminodes 0 absent48. Stamen base 0 short, 1 long wide, 2 long narrow 1/2 1/2 0/1/2 0/1/2 1/2 1/2 1/2 1/249. Paired basal stamen glands 0 absent, 1 present 0 absent50. Connective apex 0 extended, 1 truncated, 2 peltate 0 0 0 0 0/1 0/1 0 051. Pollen sacs 0 protruding, 1 embedded 0 protruding52. Microsporangia 0 four, 1 two 0 four53. Orientation 0 introrse, 1 latrorse, 2 extrorse 0/1 0/1 0/1 0/1 0 0 0 054. Dehiscence 0 longitudinal slit, 1 H-valvate, 2 fl aps 0 longitudinal slit74. Carpel number 0 more than one, 1 one 0 more than one75. Carpel form 0 ascidiate, 1 intermediate, 2 plicate 0 ascidiate76. Postgenital fusion 0 none, 1 partial, 2 complete 0 none77. Secretion 0 present, 1 absent 0 present78. PTTT a 0 not differentiated, 1 differentiated, 2 multilayered 0 not differentiated79. Style 0 absent, 1 present 0 0/1 0/1 0/1 0 0/1 0 0/180. Stigma 0 extended, 1 restricted 0 extended81. Stigmatic protuberances 0 absent, 1 present 0/1 0 0/1 0 0/1 0 0/1 082. Stigmatic papillae 0 none, 1 unicellular, 2 pluricellular 1/2 uni/pluricellular83. Extragynoecial compitum 0 absent, 1 present 0 present84. Fusion 0 apocarpous, 1 paracarpous, 2 eusyncarpous 0 apocarpous85. Oil cells 0 not visible, 1 intrusive 0 not visible86. Unicellular hairs on carpels 0 absent, 1 present 0 absent87. Curved hairs on carpels 0 absent, 1 present 1 0/1 1 0/1 0 0/1 0 0/188. Abaxial nectaries 0 absent, 1 present 0 absent89. Septal nectaries 0 absent, 1 present 0 absent90. Ovule number 0 one, 1 mostly two, 2 more than two 0 0 0/2 0/2 0 0 0 091. Placentation 0 ventral, 1 laminar-dorsal 0 ventral92. Ovule direction 0 pendent, 1 horizontal, 2 ascendent 0 pendent93. Ovule curvature 0 anatropous, 1 orthotropous 0/1 0 0/1 0 0/1 0 0/1 0

Table 1. Most parsimonious ancestral states for all characters concerning infl orescence and fl oral structure (see Appendix 1 for complete defi nitions), given different backbone trees (D & E vs. J/M), rooting with Amborella alone sister to all other angiosperms (A, N) vs. Amborella and Nymphaeales forming basal clade (A+N), and Recent taxa only vs. Recent taxa and fossil Archaefructus (R, F). When the reconstructed ancestral state is identical for all trees, it is given only once.

a pollen tube transmitting tissue.


In contrast, with the J/M backbone tree, in which Cerato-phyllum is divorced from Chloranthaceae and associated with eudicots, it is more parsimonious to associate Archaefructus with Ceratophyllum , based on dissected leaves (20), dichoto-mous venation (18), loss of fl oral bracts (25), unisexual fl owers (26), and loss of perianth (31). This position is four steps less parsimonious with the D & E backbone, where Ceratophyllum is associated with Chloranthaceae, which have more features that confl ict with those of Archaefructus , such as opposite leaves (9), pinnate venation (17), round pollen (61), and reticulate tec-tum (66). Better evidence on the position of Ceratophyllum could therefore have an impact on the best interpretation of Ar-chaefructus . Our results also depend on uncertain assumptions concerning the morphology of the fertile structures of Archae-fructus . When the fertile shoot is interpreted as a fl ower or pre-fl ower ( Sun et al., 2002 ), which we regard as unlikely, one of the most parsimonious positions of Archaefructus is still with Hydatellaceae, but it is equally parsimonious to place it else-where in Nymphaeales. Confi rmation of the view of Ji et al. (2004) that the seeds of Archaefructus were orthotropous would increase the relative parsimony of a link with Ceratophyllum .

Some of the evidence for a relationship of Archaefructus with Hydatellaceae comes from the report by Sun et al. (2001 , 2002 ) of boat-shaped, tectate monosulcate pollen grains in Ar-chaefructus , which was questioned by Friis et al. (2003) . With the D & E backbone, removal of pollen characters weakens the connection of Archaefructus with Hydatellaceae and favors a link with the eudicot genus Euptelea , supported in part by ab-sence of a perianth (31) and one stamen whorl (43), as well as palmate venation (17), shared with eudicots as a whole, and several ovules (90), a synapomorphy of mesangiosperms other than Chloranthaceae and Ceratophyllum . The possibility that Archaefructus was related to eudicots was raised by Friis et al. (2003) , based especially on the ternate, dissected leaf architec-ture. Such a relationship would imply that Archaefructus had tricolpate rather than monosulcate pollen, which would be sur-prising in light of its Barremian-Aptian age, when tricolpate pollen was exceedingly rare outside northern Gondwana ( Doyle, 1992 ; Hughes, 1994 ; Hochuli et al., 2006 ). However, even in the absence of pollen characters, relationships with Hydatel-laceae and Ceratophyllum remain almost as parsimonious with the D & E backbone, and the link with Ceratophyllum is strength-ened with the J/M backbone. These results underline the need for more convincing evidence on pollen of Archaefructus .

Our analysis does not address the hypothesis that Archae-fructus is a stem relative of all living angiosperms rather than a member of the crown group ( Sun et al., 2002 ): it only specifi es the most parsimonious position(s) of Archaefructus if it belongs in the crown group. However, the crown group hypothesis was supported by an analysis of living and fossil seed plants (Doyle, 2008), including all the ANITA lines, Chloranthaceae, and three magnoliids. When Archaefructus was interpreted as hav-ing an infl orescence of unisexual fl owers, its most parsimoni-ous position was with Hydatellaceae, and a position sister to all living angiosperms was fi ve steps worse. When the fertile axis was interpreted as a bisexual fl ower, it was again more parsimo-nious to place Archaefructus in Nymphaeales than below living angiosperms, but by three steps rather than fi ve.

Rudall et al. (2007) cited the order of fertile parts in Archae-fructus (stamens basal, carpels apical) as an argument against a relationship with Hydatellaceae, where the female fl owers in spe-cies with bisexual infl orescences are to the outside (assumed to be basal) and male fl owers are central (apical). However, if

Archaefructus has racemes and Hydatellaceae have modifi ed thyrses, as Rudall et al. (2007) argued, the order of fl owers in the two groups cannot be so easily compared. If the main axis of the infl orescence in Hydatellaceae (as reconstructed by Rudall et al., 2007 , in fi g. 5D) is compared with the main axis in Archaefruc-tus , there is no difference in the relative position of male and fe-male fl owers in the two groups. In both, the male fl owers (plus female fl owers in Hydatellaceae) are borne on more basal lateral units (cymes in Hydatellaceae), while the more distal lateral units are entirely female. Furthermore, the argument that an opposite order of male and female fl owers precludes a relationship is not compelling because analogies with other groups suggest that the order of fl owers in bisexual infl orescences can reverse. For ex-ample, in Buxaceae, male fl owers are basal and female fl owers terminal in Buxus and Styloceras kunthianum , female basal and male apical in Sarcococca and Pachysandra , and infl orescences are unisexual in other Styloceras species. Based on inferred phy-logenetic relationships ( von Balthazar and Endress, 2002b ), ei-ther one or the other bisexual condition could be ancestral, but the other bisexual type would be derived from it.

Ancestral fl oral states and initial specializations — In the following sections, we consider the ancestral state reconstruc-tions in Table 1 and their general implications. Contrary to some expectations (e.g., Qiu et al., 2006 ), trees in which Ambo-rella is sister to all other angiosperms and those in which it is linked with Nymphaeales have only modestly different impli-cations for ancestral states: all seven differences involve cases in which the ancestral state is equivocal with one rooting and one of the same two states with the other. Addition of Archae-fructus has even less impact, with a few important exceptions to be discussed. Finally, except for the positions of Chloranthaceae and Ceratophyllum , the differences between arrangements of mesangiosperm lines in the D & E combined and J/M plastid trees ( Jansen et al., 2007 ; Moore et al., 2007 ) have generally minor effects. This result seems due to two factors. First, infer-ences on ancestral states are most dependent on relationships in the ANITA grade, which are the same with both arrangements. Second, very few morphological changes occurred on the inter-nodes between the three main lineages of mesangiosperms (magnoliids, eudicots, and monocots), however they are ar-ranged, presumably because these lineages radiated in a very short time ( Moore et al., 2007 ), the same reason their relation-ships have been so diffi cult to resolve.

Infl orescence organization — Because of varying views on interpretation of fl owers and infl orescences in taxa such as Ar-chaefructus , Hydatellaceae, and Chloranthaceae and recent suggestions that the distinction between infl orescences and fl owers may be labile or problematic in basal angiosperms ( Friis and Crane, 2007 ; Rudall et al., 2007 ), we have considered char-acters of infl orescences as well as fl owers.

Based on our results, with Amborella basal ( Fig. 3 ), the an-cestral infl orescence type (character 22 ) in angiosperms is equivocal: either botryoids, as in Amborella ; or racemes (which some authors might describe as stems with solitary axillary fl owers), as in Nymphaeales, Chloranthaceae (modifi ed to spikes and thyrses), and basal eudicots and monocots. However, if Amborella is linked with Nymphaeales, the ancestral type can be reconstructed as a raceme. Both hypotheses imply that soli-tary fl owers, often considered ancestral in angiosperms, are in-stead derived: from racemes in Austrobaileyales (with a shift to botryoids in Trimenia ), magnoliids, and Nelumbo , and from


the base of the pedicel, but she argued that the Nuphar condition is derived, as a result of intercalary growth between the abaxial tepal and the rest of the fl ower. This interpretation is less plausi-ble in terms of outgroup comparison. We have therefore scored both Nuphar and Nymphaeoideae ( Nymphaea , Euryale , and Vic-toria ) as having racemes, with the fl oral subtending bract present in Nuphar but absent in Nymphaeoideae (which could be due either to reduction or to incorporation into the perianth). The condition in Barclaya is unknown, although it appears consistent with that in Nuphar and Nymphaea .

From this perspective, the whole shoot system of Nymphae-aceae can be considered a giant raceme. If the pherophyll-bud primordium is viewed as a complex of two parts (cf. Chassat, 1962 ), in some cases, the pherophyll part develops into a foliage leaf, and the fl oral bud is suppressed; in others, the fl oral bud grows rapidly after initiation, and the pherophyll is reduced to a thin bract or nothing at all. One could also suggest there is com-petition for space: either the fl ower or the leaf is reduced, and the other, more precocious part “ wins. ” This divergence in develop-ment may be a function of the gigantism of the shoots, leaves, and fl owers of these plants, compared to their outgroups.

Victoria and Euryale may provide indirect support for this interpretation. Borsch et al. (2007) identifi ed these taxa as the sister group of Nymphaea , but subsequent analyses of more markers ( L ö hne et al., 2007 ) indicate they are nested within Nymphaea and are therefore unlikely to represent the ancestral condition in Nymphaeaceae. However, they too can be inter-preted in terms of an underlying racemose pattern. In Victoria and Euryale the fl owers arise in a Fibonacci spiral. Each fl ower is associated with a leaf, but it is located not in the middle of the leaf axil but rather toward the inner side, in terms of the direc-tion of the spiral (anodic side; Cutter, 1961 ; Schneider et al., 2003 ). Cutter (1961) described the leaves and fl owers as form-ing two separate spirals, but an interpretation more consistent with normal angiosperm morphology may be that each fl ower is in the axil of a foliage leaf but slightly displaced ( Chassat, 1962 ). This displacement might be due to the fact that both leaf (petiole) and fl ower (pedicel) are bulky, so an exact superposi-tion would not allow enough space in the mature state. As in Nymphaea , the abaxial tepal in Victoria develops fi rst; but the fact that Victoria has a subtending leaf as well could be evi-dence against identifi cation of the abaxial tepal in Nymphaea with the fl oral subtending bract. Because each pherophyll de-velops into a leaf and each bud develops into a fl ower, the num-ber of fl owers and leaves in a shoot is the same. In contrast, in Nuphar and Nymphaea only the leaf or only the fl ower of the pherophyll/fl ower “ complex ” develops to maturity, and the numbers of mature fl owers and leaves in a shoot are not neces-sarily equal. If Victoria and Euryale are nested in Nymphaea , in which the subtending leaf is absent, their condition may repre-sent a “ reactivation ” of the pherophyll portion of the leaf-bud primordium, perhaps related to even more extreme gigantism.

In Hydatellaceae, interpretation of the crowded infl ores-cences of extremely simple fl owers is made diffi cult by the lack of subtending bracts for the lateral branches. However, Rudall et al. (2007) tentatively but plausibly interpreted the fl owers as forming reduced thyrses.

Based on the inferred phylogenetic relationships, racemes are ancestral in Nymphaeales, either as a synapomorphy or a retention from the fi rst angiosperms. With bracts present in Cabomba and Nuphar , it is most parsimonious to assume that bracts were lost independently on the line to Hydatellaceae and Archaefructus (if these two taxa form a clade) and within

botryoids in the Hydrastis - Glaucidium clade in Ranunculaceae. In magnoliids, solitary fl owers may have evolved either once from racemes at the base of the Magnoliales-Laurales clade, with a reversal in Myristicaceae and a shift to botryoids in Lau-rales, or separately from racemes in Magnoliales and from ei-ther racemes or botryoids in Laurales (Calycanthaceae).

Thyrses, distinguished from racemes and spikes by the lateral unit character ( 23 ; cymes rather than single fl owers), appear to be derived from racemes in Hydatellaceae, Chloran-thaceae, Aristolochioideae, and Butomus , and from either ra-cemes or botryoids in Siparunaceae and Hernandiaceae. Sessile fl owers ( 24 ) were derived from pedicellate ones, resulting in spikes in Chloranthaceae and Ceratophyllum (a synapomorphy with the D & E backbone, a convergence with the J/M back-bone), the Piperaceae-Saururaceae clade, monocots (separately in Acorus , Araceae, and Aponogeton ), and Platanus (modifi ed into heads), and botryoids with sessile fl owers (i.e., stachyoids) in Tetracentron . In all these cases, reduction of the pedicel is correlated with general fl oral reduction. Loss of bracts ( 25 ; ar-rows in Fig. 3 ) occurred in several lines in which racemes were modifi ed to spikes ( Hedyosmum and Ceratophyllum , either once or twice, depending on backbone tree and optimization; Acorus , Araceae, Aponogeton , Platanus ) or thyrses of reduced pedicellate fl owers (Hydatellaceae) and might also seem corre-lated with reduced fl owers. However, this is not a universal rule because bracts were also lost within Nymphaeaceae, in which fl owers are unusually large.

Nymphaeales deserve special attention because interpreta-tion of their infl orescence morphology is both particularly con-troversial and potentially relevant to ancestral conditions and early trends in angiosperms. Cutter (1957a , b , 1959 , 1961 ) de-scribed Nymphaeaceae ( Nuphar , Nymphaea ) as having a unique system of solitary fl owers borne in the same phyllotactic spiral as leaves, with no subtending bracts (accepted by Schneider et al., 2003 ), which she compared with conditions in ferns. This view was critiqued by Chassat (1962) , who interpreted Nympha-eaceae as having modifi ed racemes, with the apparent position of fl owers in the same spiral as leaves due to reduction of the leaf (pherophyll) component of a leaf-bud primordium.

In a phylogenetic context, with Cabombaceae sister to Nymphaeaceae, the interpretation of Chassat (1962) makes more sense because Cabomba has racemes, with fl owers borne in the axils of peltate fl oating leaves ( Brasenia has not been studied in suffi cient detail for comparisons). It would also bring Nympha-eaceae in line with the normal shoot organization in angiosperms and other seed plants. Closer examination of infl orescence and fl oral morphology in Nymphaeaceae supports this view. Nuphar , which is basal in Nymphaeaceae, has a bract near the base of the pedicel, on its abaxial side with respect to the main axis and thus near the position of a subtending bract, and three outer tepals. Nymphaea , however, has no bract on the pedicel and four outer tepals, with the fi rst-formed tepal abaxial relative to the main axis, like the bract in Nuphar . As discussed by Chassat (1962) , this structure might be derived from that in Nuphar either by complete reduction of the subtending bract or by its incorpora-tion into the perianth as the abaxial tepal. The latter hypothesis would explain the change from trimerous to tetramerous organi-zation of the perianth. On the other hand, the earlier development of the abaxial tepal could be a function of the fact that the fl ower is more developed on the abaxial side at the time the tepals are initiated and somewhat incurved. Cutter (1957b) also homolo-gized the bract in Nuphar with the abaxial tepal in Nymphaea , noting cases in Nymphaea in which this tepal is displaced toward


leading to the remaining mesangiosperms is bisexual. With the J/M backbone and Amborella basal, the state is equivocal up to the node connecting Nymphaeales and the remaining groups. Rescoring Archaefructus as uncertain (0/1) for this character based on the report of bisexual units by Ji et al. (2004) would not modify these inferences.

The view that bisexual fl owers were ancestral is supported by the regular presence of one or two sterile stamens in female fl owers of Amborella ( Endress and Igersheim, 2000b ; Buzgo et al., 2004 ). In other words, the fl owers are organizationally bi-sexual. Michael Frohlich, Royal Botanic Gardens, Kew (per-sonal communication) also gave us a likelihood argument in support of the view that the unisexual state in Amborella is de-rived, namely that Amborella terminates a long branch with no surviving side-branches, whereas the sister branch (including all the remaining angiosperms) is “ broken up ” by several lin-eages near its base. This difference in branch length could mean that inference of the initial state is more secure on the latter line

Nymphaeaceae ( Nymphaea ). Archaefructus still had racemes, but these were modifi ed into thyrses in Hydatellaceae, by re-placement of single lateral fl owers by cymes. One possible adaptive explanation is that the resulting increase in number of fl owers compensated for the reduction in number of carpels and ovules, but the small number of cymes in the living group may refl ect a later round of reduction.

Floral organization — In recent years most authors have as-sumed that the fi rst angiosperms had bisexual fl owers ( 26 ), but because the fl owers of Amborella are functionally unisexual the ancestral state is equivocal. With our previous data set, the lin-eage leading to all other angiosperms could be reconstructed as basically bisexual, but the situation has changed with the addi-tion of Hydatellaceae (and Archaefructus , if it is linked with Hydatellaceae). With the D & E backbone, the state is equivocal up to the basal node of the mesangiosperms, above which the Chloranthaceae- Ceratophyllum line is unisexual and the line

Fig. 3. D & E tree of Recent taxa, with coloring of branches showing most parsimonious course of evolution of infl orescence character (22; state 1 = botryoid, panicle, or thryrsoid; state 2 = raceme, spike, or thyrse). Boxes under names of taxa indicate their character state; colors of branches indicate their reconstructed state based on parsimony optimization. Arrows indicate losses of fl oral subtending bracts (character 25) and possible states on branches where parsimony optimization is equivocal (e.g., 0/2 = either solitary fl ower or raceme). Position and number of losses of bracts in Ceratophyllum and Chloranthaceae are equivocal. Abbreviations as in Fig. 2 .


Fig. 4. (A) D & E tree, showing inferred evolution of perianth phyllotaxis (character 32). Arrows indicate loss of perianth (character 31); position and number of losses in Ceratophyllum and Chloranthaceae are equivocal. (B) Inferred evolution of perianth merism (character 33); taxa with spiral phyllotaxis scored as unknown. Abbreviations as in Fig. 2 .


perianth). Independent losses occurred in Hydatellaceae (with or without Archaefructus ), the Piperaceae-Saururaceae clade, the strange case of Eupomatia (and Galbulimima if its outer petaloid organs are staminodes; we scored perianth as unknown, but it is probably absent), and Euptelea (arrows in Fig. 4A ). Loss of the perianth in Ceratophyllum and Chloranthaceae other than Hedyosmum poses more problems. The analyses of Doyle and Endress (2000) and Eklund et al. (2004) indicated that the presence of three tepals in Hedyosmum was plesiomor-phic and their loss a synapomorphy of other Chloranthaceae, and this is still so for the J/M tree. However, if Ceratophyllum is related to Chloranthaceae, as in the D & E tree ( Fig. 4A ), and if we are correct in interpreting Ceratophyllum as lacking a pe-rianth, it is equivocal whether the perianth of Hedyosmum is a primitive retention or a secondary invention.

As discussed in Endress and Doyle (2007) , the ancestral pe-rianth phyllotaxis ( 32 ; Fig. 4A ) is equivocal: either the spiral state of Amborella and Austrobaileyales is ancestral and the whorled state of Nymphaeales is derived, or vice versa. How-ever, the reconstructed ancestral state in mesangiosperms is un-ambiguously whorled (see also Zanis et al., 2003 ). Cases of spiral perianth in magnoliids, once widely assumed to be primi-tive, are therefore derived from whorled: in Degeneria in the Magnoliales, and once, twice, or three times in Laurales. In the eudicots, shifts to spiral occurred in Circaeaster , core Ranun-culaceae, and Nelumbo . If a spiral perianth originated once at the base of Laurales and was retained into Calycanthaceae, Atherospermataceae, Gomortega , and the monimiaceous genus Hortonia , there was yet another round of reversal, from spiral to whorled, in other Monimiaceae and the Lauraceae-Hernandi-aceae clade. As argued by Endress (1987a) , perianth phyllotaxis is therefore a highly labile character, although it is stable over large parts of the tree.

Tracing the evolution of perianth merism ( 33 ; Fig. 4B ) is potentially confused by the occurrence of many taxa with spiral phyllotaxis, in which merism was scored as unknown but parsi-mony optimization implicitly treats taxa as having the state of the surrounding groups (cf. Maddison, 1993 ). Based on those taxa that are whorled, if the ancestral angiosperms had a whorled perianth, it was trimerous. It became polymerous within Nymphaeaceae (specifi cally tetramerous) and in Hernandiaceae (Gyrocarpoideae, some Hernandioideae), dimerous in Winter-aceae. Whether the shift from trimerous to tetramerous perianth in Nymphaeaceae was a result of incorporation of the bract into the perianth, as discussed, would be an intriguing topic for evo-devo studies. Most interesting is the case of eudicots, in which the reconstructed ancestral state is either trimerous, as in most Ranunculales, or dimerous (a possibility fi rst emphasized by Drinnan et al., 1994 ), as in Papaveraceae, near the base of Ra-nunculales, and in Proteaceae, Tetracentron ( Chen et al., 2007 ), and Buxaceae (von Balthazar and Endress, 2002a), on the line leading to “ core ” eudicots ( Gunneridae , including Pentapeta-lae , of Cantino et al., 2007 ).

The fact that trimery is reconstructed as homologous in Hedyosmum (with three tepals) and other groups ( Fig. 4B ) might be questioned as an artifact of the Maddison long dis-tance effect ( Maddison, 1993 ). With the J/M backbone, where the presence of a perianth in Hedyosmum is reconstructed as ancestral, this poses no problem. However, with the D & E back-bone ( Fig. 4B ), where Chloranthaceae are linked with Cerato-phyllum , the perianth of Hedyosmum may be a secondary invention, and if so its trimery would not be strictly homolo-gous with trimery in other taxa. On the other hand, it might be

than on the longer line leading to Amborella . However, this ar-gument is weakened by the addition of Hydatellaceae (either with or without Archaefructus ) to Nymphaeales.

An intriguing case concerns Chloranthaceae, in which Hedyosmum and Ascarina have unisexual fl owers, but Sarcan-dra and Chloranthus have bizarre bisexual fl owers consisting of one carpel and one stamen or tripartite androecium ( Endress, 1987b ; Eklund et al., 2004 ). Molecular studies and the morpho-logical analysis of Eklund et al. (2004) agree that Hedyosmum and Ascarina diverged successively below Sarcandra and Chloranthus . In Eklund et al. (2004) , in which Chloranthaceae were nested among bisexual taxa, there were two equally parsi-monious scenarios: either bisexual fl owers were plesiomorphic for the family and became unisexual independently in Hedyos-mum and Ascarina , or fl owers became unisexual in the ancestor of the family and reverted to bisexual in Sarcandra and Chlo-ranthus ( Doyle et al., 2003 ). This is still true in trees with the J/M backbone ( Fig. 2B ). However, in trees with the D & E back-bone ( Fig. 2A ), where Chloranthaceae are linked with Cerato-phyllum , which has unisexual fl owers, it is most parsimonious to assume that the bisexual fl owers of Sarcandra and Chloran-thus were derived from unisexual fl owers. In “ higher ” angio-sperm groups, we know of no cases where phylogenetic analyses imply that bisexual fl owers are derived, but it would be danger-ous to assume this was true during the early angiosperm radia-tion. In any case, it appears that fl oral sexuality was highly labile in early angiosperms. At least eight reversals from bi-sexual to unisexual also occurred within magnoliids and basal eudicots: in Lactoris (some fl owers), Myristicaceae, Sipar-unaceae, Mollinedioideae and Monimioideae (once or twice), Lardizabalaceae, Menispermaceae, Platanus , and Buxaceae.

Congenital fusion of all outer fl oral parts into a hypanthium ( 27 ) occurred independently in Amborella (where it could be either ancestral or derived if Amborella alone is basal, but de-rived if Amborella and Nymphaeales form a clade), Eupomatia , and Laurales, where it is an important synapomorphy of the order. We treated inferior ovary as a state of the same character, on the grounds that it might originate by fusion of either sepa-rate outer parts or an existing hypanthium to the ovary. The latter process does appear to have occurred in Laurales, where Gomortega and the clade consisting of Lauraceae (where the ancestral state appears to be inferior, as in Hypodaphnis and other basal genera: Rohwer and Rudolph, 2005 ) and Hernandi-aceae are nested within the order. However, there is no phylo-genetic evidence for this in the other lines with an inferior ovary ( Barclaya plus Nymphaeoideae, Hedyosmum , Saururaceae, Aristolochiaceae, Dioscoreaceae, and Trochodendraceae), whose closest outgroups have no hypanthium.

An elongate receptacle ( 28 ), often presented as a primitive feature, appears instead to be an independent advance of Schisandraceae, Magnoliaceae, and Galbulimima . In Magnoli-aceae this coincided with origin of cortical vasculature ( 29 ) extending from the perianth into the gynoecium, a feature that arose independently in Glaucidium . Cortical vasculature ex-tending only into the androecium arose before an elongate re-ceptacle in the Degeneria - Galbulimima clade and independently in Trochodendron . Protrusion of the fl oral apex ( 30 ), a dis-tinctive feature of Nymphaeoideae and Illicium , is an indepen-dent advance in these two groups.

Perianth — Our results indicate that presence of a perianth ( 31 ) is ancestral, even with the addition of Archaefructus , which has no perianth (both of its potential extant relatives also lack a


Fig. 5. (A) D & E tree, showing inferred evolution of number of perianth whorls (series in taxa with spiral phyllotaxis; character 34). (B) Inferred evolu-tion of tepal differentiation (character 35; state 1 = outer sepaloid, inner petaloid). Abbreviations as in Fig. 2 .


At least basal fusion of the outermost perianth parts ( 38 ) oc-curred independently in several lines: Amborella (there is a short zone of fusion among tepals before fusion with the sta-mens begins), Cabomba (Endress, 2008a), Canellales and Aris-tolochiaceae (either once or twice), Myristicaceae, and Degeneria (Magnoliales). On parsimony grounds, the tepal fu-sion in Amborella could be ancestral if Amborella is sister to all other angiosperms, but it is derived if Amborella and Nympha-eales form a clade. This fusion is not related to formation of a calyptra ( 39 ), apparently derived from one or two fl oral bracts ( Endress, 1977 , 2003 ; Kim et al., 2005a ), which intriguingly arose either once or three times in other Magnoliales (Magnoli-aceae, Galbulimima , Eupomatia ). At the level of angiosperms as a whole, fusion tends to be much more labile in sepals (or outer tepals) than in petals. This phenomenon is refl ected by the fact that the contrast of choripetaly vs. sympetaly has been commonly regarded as signifi cant at the macrosystematic level, whereas chorisepaly vs. synsepaly has been relatively neglected. Among basal angiosperms, tepal fusion may be interesting within genera or families, for example in Hedyosmum , where it unites a large derived clade ( Eklund et al., 2004 ). Another inter-esting feature concerns the fate of tepals after anthesis in the ANITA grade: caducous during or at the end of anthesis (com-bined with narrow attachment areas) in Austrobaileyales, but persistent (combined with broad attachment areas) in Ambo-rella and Nymphaeales (Endress, 2008a). This feature has not been explored throughout basal angiosperms and was therefore not used in our analysis. However, a caducous perianth may be a synapomorphy of Austrobaileyales. The cases of tepal fusion appear to be restricted to clades with persistent tepals.

Androecium — Our results indicate that the single stamen ( 40 ) of Hydatellaceae, Ceratophyllum , and most Chloran-thaceae is derived and is a synapomorphy of Ceratophyllum and Chloranthaceae with the D & E trees. Our data imply that the presence of a few stamens in some species of Ascarina (scored as 0/1) and the tripartite androecium of Chloranthus (scored as unknown) were derived within Chloranthaceae. This inference is sensitive to the interpretation of the androecium of Chloran-thus , which has been variously considered a result of lobation of one stamen or fusion of three ( Endress, 1987b ; Doyle et al., 2003 ). If Chloranthus is rescored as having more than one sta-men, and if Ceratophyllum is not related to Chloranthaceae (as in the J/M topology), the inferred ancestral state for the family is equivocal. However, if Ceratophyllum is associated with Chloranthaceae, one stamen is reconstructed as ancestral.

Stamen phyllotaxis ( 41 ; Fig. 6A ) is generally correlated with perianth phyllotaxis, but this correlation breaks down in Magnoliales ( Endress and Doyle, 2007 ). As with the perianth, the ancestral stamen phyllotaxis is equivocal, and with the D & E topology the basic state for the magnoliid-monocot-eudicot clade (mesangiosperms other than Chloranthaceae and Cerato-phyllum , which cannot be scored) is whorled. However, Mag-noliaceae have a whorled perianth (except for some probably derived species of Magnolia ) but spiral (or somewhat irregu-larly arranged) stamens. Stamens are also spiral in Eupomatia and Galbulimima (which have no perianth), as are both tepals and stamens in Degeneria . Myristicaceae have three whorled tepals, but their fused stamens vary between spiral and whorled (scored as 0/1). As a result, stamen phyllotaxis in magnoliids appears to have shifted to spiral earlier than perianth phyl-lotaxis, in the common ancestor of Magnoliales and Laurales, with reversals to whorled in Annonaceae (often becoming

that the reappearance of a perianth in trimerous form was a con-sequence of reactivation of an existing but suppressed develop-mental program and therefore homologous at a more fundamental genetic level (cf. Li et al., 2005 ). This reappearance of trimery could be an intriguing topic for developmental genetic research (cf. “ biological homology ” of Wagner, 1989 , 2007 ). But even if the inferred homology of the trimerous perianth in Hedyosmum is an artifact, it would still be valid to conclude that trimery is ancestral in angiosperms (if they were originally whorled) be-cause this is also inferred if Hedyosmum is deleted.

The ancestral number of perianth whorls (series when spi-ral) ( 34 ) is reconstructed as more than two, and this was re-tained from the fi rst angiosperms into magnoliids ( Fig. 5A ). The number of whorls was reduced to two in Cabombaceae, Lauraceae, and (independently or as a synapomorphy with Lauraceae) some Hernandiaceae. With the D & E backbone ( Fig. 5A ), a shift to two whorls is a conspicuous synapomor-phy of monocots and occurred two or three times in eudicots — once in Ranunculaceae, and once or twice in the other branch, depending on whether the numerous series in Nelumbo are an-cestral or derived. However, with the J/M backbone, where monocots, Ceratophyllum , and eudicots form a clade, reduc-tion to two whorls may be either an event that occurred three or four times, or a synapomorphy of these groups, with two reversals in eudicots. In Ranunculaceae, reduction to two whorls appears to have been a step toward reduction to one in Hydrastis , and the same may have occurred in Gyrocar-poideae. But one whorl was apparently derived directly from more than two in Hedyosmum (if its perianth is ancestral in Chloranthaceae), the Lactoris -Aristolochiaceae clade, Myris-ticaceae, and Circaeaster .

The inferred ancestral state of perianth differentiation ( 35 ; Fig. 5B ) is either all sepaloid tepals, as in Amborella , or outer sepaloid and inner petaloid tepals, the basic state in the line lead-ing to all other angiosperms. If Amborella is linked with Nymphaeales, the differentiated state is unequivocally ancestral. Tepals became all sepaloid in Trimenia and one to three times in Laurales. As with the origin of two perianth whorls, with the D & E trees tepals became all sepaloid in monocots and once or twice in eudicots ( Platanus , Proteaceae, Tetracentron , and Buxaceae), depending on whether the differentiated tepals of Nelumbo are ancestral or derived, but with the J/M trees this is a possible synapomorphy of the two clades. Differentiated tepals became all petaloid in Cabombaceae and some Ranunculales. In monocots, the all petaloid state is a synapomorphy of the “ core ” monocot clade represented by Dioscoreaceae, Nartheciaceae, and Melanthiaceae ( Petrosaviidae of Cantino et al., 2007 ), apparently derived from all sepaloid. True petals ( 36 ) are a sy-napomorphy of Ranunculales other than Euptelea , with conver-gent origins in Nuphar and within Asaroideae ( Saruma ). The adaxial nectar glands ( 37 ) on the inner petals of many Ranun-culales apparently originated once after origin of petals, after divergence of Papaveraceae, with a convergence in Cabomba .

If core eudicots ( Gunneridae of Cantino et al., 2007 ) are linked with Buxaceae and/or Trochodendraceae ( Soltis et al., 2003 ), our results support the hypothesis that the typical dicy-clic, pentamerous perianth of the gunnerid groups other than Gunnerales ( Pentapetalae of Cantino et al., 2007 ) was derived from two dimerous whorls of reduced sepal-like organs (con-trary to Wanntorp and Ronse De Craene, 2005 ). Whether this occurred by increase in the number of parts per whorl or by ad-dition and reorganization of new whorls is beyond the scope of this paper.


Fig. 6. (A) D & E tree, showing inferred evolution of androecium phyllotaxis (character 41). (B) Inferred evolution of number of stamen whorls (series in taxa with spiral phyllotaxis; character 43). Abbreviations as in Fig. 2 .


Eupomatia , and Annonaceae (where inner staminodes are re-tained in the basal genus Anaxagorea ; Maas and Westra, 1984 ; Scharaschkin and Doyle, 2006 ). Glandular food bodies ( 47 ) on the inner staminodes are a more secure synapomorphy of the Degeneria -Annonaceae clade.

“ Laminar ” or “ leafl ike ” stamens have often been considered ancestral in angiosperms (e.g., Canright, 1952 ). However, the fact that the sporangia are adaxial in some laminar stamens and abaxial in others suggests that the laminar condition may not be homologous across basal angiosperms. This led Takhtajan (1969) to suggest that the ancestral stamen had marginal spo-rangia, a condition usually associated with a narrow connec-tive. Rather than contrasting laminar and fi lamentous, we have split stamen morphology into several characters.

One character concerns the stamen base ( 48 ; Fig. 7A ), with three states: short (either wide or constricted, which often inter-grade: Eklund et al., 2004 ), long and wide, and long and narrow (= typical fi lament; see Appendix 1 for limits between states). Stamens with both of the fi rst two states have been described as laminar. With our previous data set ( Doyle and Endress, 2000 ), the ancestral state was either long and wide (as in Amborella and most Austrobaileyales) or narrow (as in Cabombaceae and Trimenia ). This is still true with Recent taxa only and both backbone topologies, because Hydatellaceae also have a long and narrow base, but with the D & E backbone and the addition of Archaefructus , which has a short base, any of the three states may be ancestral. Within Nymphaeales, there is a series from long and narrow to short to long and wide if only living taxa are considered, but if Archaefructus is linked with Hydatellaceae this becomes equivocal. With the D & E backbone, a long and narrow fi lament is basic for mesangiosperms other than the Chloranthaceae- Ceratophyllum line (most of which have a short base), and a shift to laminar stamens with a short base unites Magnoliales and Laurales. This reversed to long and nar-row in the clade consisting of Monimiaceae, Lauraceae, and Hernandiaceae. However, with the J/M backbone, the state at the base of mesangiosperms is entirely unresolved, and the short base of Magnoliales and basal Laurales may be either de-rived or inherited from lower in the tree.

Paired basal glands ( 49 ), a peculiar feature of the stamens of many Laurales, originated either once after divergence of Calycanthaceae, with reversals in Siparunaceae and Molline-dioideae, or twice, in the Atherospermataceae- Gomortega and Monimiaceae-Lauraceae-Hernandiaceae clades. Given the dis-tinctive nature of this advance and the fact that its absence in Siparunaceae and Mollinedioideae is correlated with packing of the stamens in a deep hypanthium, the former scenario may be more likely.

An extended connective apex ( 50 ) is also common in lami-nar stamens. As in Doyle and Endress (2000) , this feature is ancestral on most trees, except the J/M trees with Recent taxa only, where the ancestral state is equivocal. If the extended type is ancestral, truncation of the apex occurred an uncertain num-ber of times in four near-basal lines (Hydatellaceae, Cabom-baceae, Schisandraceae plus Illicium , and Sarcandra ) and in mesangiosperms. With the D & E backbone a truncated apex is reconstructed as basic for the monocot-magnoliid clade, and in all trees it is ancestral in magnoliids. As a result, the extended apex of the classic laminar stamens of Magnoliales is a second-arily derived feature that unites Galbulimima , Degeneria , Eupomatia , and Annonaceae, and in Laurales the same is true for Calycanthaceae. The situation is confused in eudicots: it is equivocal whether the extended apex of Euptelea , Nelumbo ,

chaotic within the androecium: Endress, 1987a ) and either once or twice in Mollinedioideae and the Lauraceae-Hernandiaceae clade. With the J/M backbone, because whorled eudicots and monocots are consolidated in a clade and Chloranthaceae are linked with magnoliids, the ancestral state in mesangiosperms is equivocal, and it is possible that the spiral androecium in Magnoliales and Laurales was retained from the fi rst angio-sperms, rather than being a reversal or a convergence with Am-borella and Austrobaileyales, as we inferred for the perianth. A less consequential discrepancy between perianth and androe-cium occurs in Nelumbo , where tepals are spiral but stamens are produced chaotically on a ring primordium ( Hayes et al., 2000 ; here scored as unknown).

As with the perianth, a trimerous androecium ( 42 ) is pre-dominant and reconstructed as ancestral (if one assumes the androecium was originally whorled). Changes in stamen mer-ism are only sometimes correlated with those in the perianth. The androecium became polymerous before the perianth in Nymphaeaceae (before rather than after divergence of Nuphar ) and in Canellales, where the perianth remained trimerous in Canellaceae (the polymerous androecium may be related to connation of the stamens) and became dimerous in Winter-aceae. Like the perianth, the ancestral androecium in eudicots may have been either trimerous or dimerous (the latter would be favored if Euptelea is dimerous, as some have suggested, but this is unclear: Hoot et al., 1999 ; Ren et al., 2007 ).

The inferred ancestral number of stamen whorls (or series) ( 43 ; Fig. 6B ) is more than two, as in the perianth. However, in contrast to the situation in the perianth, where more than two whorls were apparently retained from the fi rst angiosperms into magnoliids, with the D & E backbone a shift to two stamen whorls occurred near the base of mesangiosperms (either above or below Chloranthaceae) and reversed to more than two in Magnoliales and Laurales ( Fig. 5B ). With the J/M backbone both this scenario and persistence of more than two stamen whorls (or series) into magnoliids are equally parsimonious (as was also true for spiral stamen phyllotaxis). With this backbone, origin of two stamen whorls may be a synapomorphy of mono-cots and eudicots, but it may equally well be homologous with the same state in Piperales and Canellaceae. Other noteworthy changes include increases from two to more than two stamen whorls (or series) in Ranunculaceae, Nelumbo , and Trochoden-dron , and reductions from more than two to one in Cabomba and Myristicaceae, from more than two to two in Hernandi-aceae, and from two to one in Euptelea and Circaeaster .

Production of stamens in double positions ( 44 ) evolved in-dependently in Nymphaeales (the condition in Hydatellaceae and Archaefructus is undefi ned), Aristolochiaceae, Annonaceae, Butomus , and Papaveraceae, and within Winteraceae, Molline-dioideae, and Tofi eldiaceae, where both states occur. At the taxonomic level of this analysis, stamen fusion ( 45 ) is a sepa-rate advance wherever it occurs (Schisandraceae, Canellaceae, Myristicaceae, Eupomatia , and within several other taxa).

The intriguing possibility that inner staminodes ( 46 ) might be a primitive feature in angiosperms ( Endress, 1984 ; Dono-ghue and Doyle, 1989 ) is not borne out: inferred relationships imply that inner staminodes originated independently in Aus-trobaileya and in Magnoliales and Laurales. In the latter groups, because we scored Myristicaceae as unknown, since they have highly modifi ed male fl owers with a central columnar androe-cium, it is equally parsimonious to assume that inner stami-noides arose once, followed by loss in Magnoliaceae, or twice, in Laurales and the clade consisting of Galbulimima , Degeneria ,


Fig. 7. (A) D & E tree, showing inferred evolution of form of stamen base (character 48). (B) Inferred evolution of orientation of anther dehiscence (character 53). Abbreviations as in Fig. 2 .


aceae, or separately in the atherosperm and Lauraceae-Hernandi-aceae clades.

In Magnoliales embedded pollen sacs, inner staminodes, food bodies, extended connective apex, and H-dehiscence ap-pear to have evolved in the context of beetle pollination, so it is interesting that some of these advances also occurred in Caly-canthaceae, another beetle-pollinated group, as early empha-sized by Grant (1950) .

Gynoecium — We have not recognized separate characters for carpel phyllotaxis and merism because these features are usually correlated with those of the androecium. The most con-spicuous deviation from this correlation is presence of one car-pel ( 74 ), which we contrast with more than one. More than one carpel is reconstructed as ancestral; reduction to one occurred independently in Hydatellaceae, Trimenia , Myristicaceae, De-generia , the Lauraceae-Hernandiaceae clade, Berberidaceae, Proteaceae, and within several groups. In the D & E trees, reduc-tion to one carpel is an important synapomorphy of Ceratophyl-lum and Chloranthaceae.

One of the most signifi cant results of the molecular rooting of angiosperms was its implication that the ancestral carpel was not the conduplicate or plicate type of Magnoliales and Winter-aceae, similar to a leaf folded down the middle ( Bailey and Swamy, 1951 ), but rather the ascidiate type, which grows up as a cup or tube as the result of a meristematic cross-zone between the primordium margins, and was sealed not by postgenital fusion but by secretion in the resulting canal ( Endress and Igersheim, 2000a ). Earlier, margins of some plicate carpels had been described as unsealed, so that pollen tubes grew to the ovules among stigmatic hairs, but in fact they are sealed by postgenital fusion of the immature epidermises ( Igersheim and Endress, 1997 ). Because these topics were discussed in detail in Doyle and Endress (2000) and Endress and Igersheim (2000a) , we consider them more briefl y here, except where the two back-bone topologies have different implications. Our conclusions are not affected by addition of Archaefructus , in which we con-servatively scored these characters as unknown, because they are often impossible to evaluate in the absence of developmen-tal or anatomical data ( Endress, 2005 ).

In all trees, the ancestral carpel form ( 75 ) is ascidiate. With the D & E backbone ( Fig. 8A ), origin of the plicate carpel is an important synapomorphy of mesangiosperms other than Chlo-ranthaceae and Ceratophyllum , with reversals to ascidiate in Mollinedioideae, Circaeaster , Berberidaceae, and Nelumbo . The intermediate type, with both ascidiate and plicate zones be-low the stigma and the ovule(s) attached to the ascidiate zone, evolved from ascidiate in Barclaya and Illicium , but also from plicate in Myristicaceae, Laurales other than Calycanthaceae, Acorus , and Euptelea . In contrast, with the J/M backbone ( Fig. 8B ), with Chloranthaceae and Ceratophyllum nested at differ-ent positions in mesangiosperms, scenarios in mesangiosperms are equivocal. Either the ascidiate carpels of Chloranthaceae and Ceratophyllum are primitive and plicate carpels originated separately in eudicots, monocots, and magnoliids, or plicate carpels originated at the base of mesangiosperms and reversed twice to ascidiate in Chloranthaceae and Ceratophyllum . In monocots, the intermediate carpels of Acorus may or may not be evolutionarily intermediate between ascidiate and plicate, and the ascidiate carpels of some Araceae may be either primi-tive or derived.

As already noted, we split modes of carpel sealing into two characters. Scenarios for origin of postgenital fusion of the

and Buxaceae is ancestral or derived. A peltate apex originated independently in Nuphar and Platanus (and within Annon-aceae: Doyle et al., 2000; Scharaschkin and Doyle, 2006 ; see also Endress, 2008b ).

Embedded pollen sacs ( 51 ) are characteristic of some lami-nar stamens, as in Degeneria , but they also occur in taxa with fi lamentous stamens, such as the Piperaceae-Saururaceae clade, and some laminar stamens have protruding pollen sacs, as il-lustrated most graphically by Austrobaileya . Protruding pollen sacs are inferred to be ancestral, as in Amborella and Austrobai-leyales, and embedded pollen sacs were derived several times, often uniting important groups: Nymphaeaceae, Chloranthaceae (reversed in Chloranthus ) and Ceratophyllum (if these are re-lated), Piperaceae-Saururaceae, Magnoliales other than Myris-ticaceae, once or twice in Laurales (in the “ atherosperm ” clade consisting of Atherospermataceae, Gomortega , and Sipar-unaceae and the Lauraceae-Hernandiaceae clade), and Trocho-dendraceae. Reduction to two microsporangia ( 52 ) occurred once (with reversals) or more times in Laurales — in the athero-sperm clade, Lauraceae (where the ancestral state is unclear: Rohwer and Rudolph, 2005 ), and Hernandiaceae, nearly coincid-ing with the shift to embedded pollen sacs — and in Circaeaster .

Orientation of dehiscence (microsporangium position) ( 53 ) is one of the most homoplastic fl oral characters (consistency index, C. I. = 0.09), but it shows some noteworthy patterns ( Fig. 7B ). Problems in scoring of unistaminate fl owers are discussed in Appendix 1. In Doyle and Endress (2000) , introrse dehis-cence (adaxial microsporangia), as in Amborella , Nymphae-aceae, and most Austrobaileyales, was ancestral, but with the addition of Hydatellaceae, which are latrorse, the ancestral ori-entation is equivocal (introrse or latrorse) in the D & E trees ( Fig. 7B ). However, with the J/M backbone, introrse is still re-constructed as ancestral, because the latrorse Chloranthaceae are further from the base of the tree. The ancestral state for me-sangiosperms is equivocal with all trees, but by the base of the magnoliids dehiscence appears to have become extrorse. These results, together with those on stamen base (48), are therefore consistent with a scenario in which the introrse laminar stamens of the fi rst angiosperms fi rst became more fi lamentous, and then these stamens were secondarily expanded with a new, abaxial microsporangium position in magnoliids. Reversals to introrse occurred in Magnolioideae, Eupomatia , and Laurales, where introrse is a synapomorphy of groups other than Caly-canthaceae (with reversals in Hortonia and Gyrocarpoideae and much plasticity in Lauraceae, often within the same fl ower). Latrorse is widespread in eudicots, perhaps functionally related to the narrow fi lament of most groups, but it is equivocal as a synapomorphy of the clade.

Anther dehiscence ( 54 ) by longitudinal slits is clearly ances-tral. Branching of the ends of the slit, resulting in “ H-valvate ” dehiscence, occurred in Nuphar , Monimioideae (Laurales), Euptelea , Platanus , within Calycanthoideae ( Sinocalycanthus ; Staedler et al., 2007 ), and as a synapomorphy of Sarcandra and Chloranthus , the Galbulimima -Annonaceae clade (Magnoliales), and Trochodendraceae. In Nymphaeales, Chloranthaceae, and Magnoliales, it appears to have evolved after embedded pollen sacs. This feature is also known from a number of unplaced Cre-taceous fossils ( Friis et al., 1991 , 2006 ) and the Late Cretaceous calycanthoid fl ower Jerseyanthus ( Crepet et al., 2005 ). Dehis-cence by apically hinged fl aps is a distinctive feature of many Laurales, but like basal glands, which have a partially overlap-ping distribution, its history is equivocal: it may have arisen after divergence of Calycanthaceae, with a reversal within Monimi-


Fig. 8. (A) D & E tree, showing inferred evolution of carpel form (character 75; state 1 = intermediate, with ovule(s) on ascidiate zone). (B) J/M tree, showing different reconstruction of evolution of same character. Abbreviations as in Fig. 2 .


reversal in the Piperales-Canellales clade. In any case, the long stigmatic crest of Degeneria , often interpreted as a primitive feature, appears to be a reversal.

Stigmatic protuberances ( 81 ), found in Amborella , may be ancestral if Amborella is basal in angiosperms, but not if Ambo-rella and Nymphaeales form a clade. Other occurrences origi-nated independently, in Trimenia , Chloranthaceae (with a loss in Sarcandra ), Idiospermum , and Hydrastis plus Glaucidium . Stigmatic papillae ( 82 ) with either a pluricellular ( Amborella , Hydatellaceae, Barclaya , Nymphaeoideae) or unicellular emer-gent portion may be ancestral, but the unicellular state was es-tablished in the common ancestor of Austrobaileyales and mesangiosperms, followed by scattered origins of pluricellular papillae in Trimenia , Asaroideae, Degeneria , Eupomatia , and Butomus , and losses of papillae in Ceratophyllum , Sarcandra plus Chloranthus , Berberidaceae, and Hydrastis .

Formation of an extragynoecial compitum ( 83 ), where con-tact between stigmas allows pollen tubes to grow to more than one carpel, appears to be ancestral in angiosperms and was re-tained through Austrobaileyales, with a loss in Cabombaceae. With the D & E backbone ( Fig. 10A ), this feature is lost near the base of the mesangiosperms (the state in Chloranthaceae is un-defi ned because they have only one carpel), followed by reap-pearances in Magnoliales and Laurales (once with a loss in Magnoliaceae, or independently in the Galbulimima -Annon-aceae clade and in Laurales) and (once or twice) in Lardizabal-aceae and Menispermaceae. With the J/M backbone, both this scenario and one in which an extragynoecial compitum per-sisted into Magnoliales and Laurales, with parallel losses in the monocot-eudicot and Piperales-Canellales clades, are equally parsimonious. Actual fusion of carpels ( 84 ; Fig. 10B ) occurred several times by two different routes. Eusyncarpy, with carpels fused at the center of the gynoecium, often resulting in axile placentation, evolved independently in Nymphaeaceae, Aristo-lochiaceae, monocots, and the Trochodendraceae-Buxaceae (and gunnerid) clade. The topology in monocots implies that the free carpels of Alismatales other than Araceae are not prim-itive but rather secondarily derived from united carpels, as con-cluded by Chen et al. (2004) . However, the situation in the Piperales-Canellales clade is confused: Aristolochiaceae are eusyncarpous (or paracarpous in some presumably derived Aristolochia species), but Piperaceae-Saururaceae, Canel-laceae, and Takhtajania in the Winteraceae ( Endress et al., 2000 ) are paracarpous, with carpels fused into a unilocular ovary with parietal placentation, and other Winteraceae and Lactoris are apocarpous. One scenario is that apocarpy was an-cestral; paracarpy originated independently in the Piperaceae-Saururaceae clade, Takhtajania , and Canellaceae; and eusyncarpy evolved from apocarpy in Aristolochiaceae. In other scenarios, paracarpy was ancestral and reversed to apocarpy in Lactoris and Winteraceae. In any case, paracarpy evolved independently in Papaveraceae.

Several minor modifi cations involve the carpel surface. In-trusive oil cells ( 85 ) visible at the carpel surface (scored only in taxa with mesophyll oil cells) originated independently in Aus-trobaileyales (Schisandraceae, Illicium , and possibly Trimenia , which is mixed), Sarcandra plus Chloranthus , the Piperaceae-Saururaceae clade, and once or twice in Monimiaceae ( Horto-nia and Mollinedioideae). Long unicellular hairs ( 86 ) on and/or between the carpels may be a synapomorphy of Laurales, but this is equivocal because they are absent in Gomortega and Si-parunaceae; similar hairs also evolved in Hydrastis and within several taxa. Short curved hairs ( 87 ) with a long apical cell

carpel margins ( 76 ) in mesangiosperms are similar to those for origin of the plicate carpel, differing with the D & E and J/M trees. However, the two characters are not redundant, because complete fusion also arose at the base of Nymphaeaceae, when the carpels were still fully ascidiate, and its history within mag-noliids, monocots, and eudicots was different. Laurales other than Calycanthaceae shifted to intermediate carpels but have complete or partial postgenital fusion, and complete fusion may have persisted into Lauraceae and Hernandiaceae. Euptelea and Acorus also have intermediate carpels but complete postgenital fusion. Many monocots (aquatic Alismatales, the Melanthi-aceae-Dioscoreales clade) are plicate but have only partial post-genital fusion, and some Ranunculales are plicate but have no or partial postgenital fusion. As a result, with the J/M backbone ( Fig. 9A ), it is equally parsimonious to assume that lack of post-genital fusion persisted well into both monocots and eudicots, even though they were plicate, or that there were reversals of postgenital fusion within these groups. Secretion in the carpels ( 77 ) persisted well into groups with plicate carpels and post-genital fusion, being lost once or twice in Canellales and Piper-ales; in Degeneria , Eupomatia , Calycanthaceae, Gomortega , and the Lauraceae-Hernandiaceae clade; and an uncertain num-ber of times in eudicots, always either coincident with or subse-quent to postgenital fusion. However, secretion was retained in monocots.

A single cell layer of pollen tube transmission tissue ( 78 ) originated repeatedly: in Austrobaileyales (once or twice: it is absent in Trimenia ), Asaroideae (Piperales), Canellales, the Galbulimima -Annonaceae clade (Magnoliales), Hortonia (Monimiaceae), monocots, and three times in eudicots (Lard-izabalaceae, Berberidaceae-Ranunculaceae, and the clade of Proteales, Trochodendraceae, and Buxaceae). However, it seems stable within these groups (except possibly Austrobai-leyales). This character needs more study, since the “ differenti-ated ” state includes more than one type of cell differentiation. Most signifi cant is a third state, multilayered transmission tis-sue, which is one of several morphological synapomorphies of Lauraceae and Hernandiaceae.

The most homoplastic character is formation of a style ( 79 ; C. I. = 0.05 – 0.06). The reconstructed ancestral state is either lack of a style (i.e., sessile stigma) or equivocal, depending on the backbone tree, the arrangement of Amborella and Nympha-eales, and addition of Archaefructus , which has a style (see Table 1 ). The basic state in mesangiosperms is presence of a style with the D & M backbone, followed by many losses (e.g., one or two in Magnoliales), but equivocal with the J/M back-bone — a style may have originated once or many times. How-ever, in some clades a style seems to have persisted once formed, as in most of the Laurales, Alismatales other than Ar-aceae, the Melanthiaceae-Dioscoreales clade (petrosaviids), and the Buxaceae-Trochodendraceae clade (probably including gunnerids). Stigma extension ( 80 ) is less homoplastic ( Fig. 9B ): a stigma extending more than halfway down the style-stigma zone is reconstructed as ancestral, and it did not become restricted to the apex until within mesangiosperms. In the J/M trees, where Chloranthaceae (with an extended stigma) are linked with magnoliids, this occurred four times, in the Magno-liales-Laurales clade, monocots, Ranunculales other than Eupt-elea (Papaveraceae scored as unknown because the stigma is modifi ed by syncarpy; reversed in Berberidaceae), and Pro-teaceae; but in the D & E trees ( Fig. 9B ), where Chloranthaceae are basal in mesangiosperms, restriction of the stigma may or may not be homologous in monocots and magnoliids, with a


Fig. 9. (A) J/M tree, showing inferred evolution of postgenital fusion of carpel margins (character 76). (B) D & E tree, inferred evolution of stigma extension (character 80). Abbreviations as in Fig. 2 .


marginal placentation in Nymphaeales (the state in Hydatel-laceae is unknown, because the fl owers lack orientation marks) and Butomus (and presumably related Alismatales). The ances-tral ovule direction ( 92 ; Fig. 12 ) is reconstructed as pendent, both in basal groups with one apical ovule, such as Amborella and Hydatellaceae, and in multiovulate Nymphaeales. Aus-trobaileyales show one or two shifts to horizontal, in Austrobai-leya and Schisandraceae, and one to ascendent, in Illicium . With the D & E tree, pendent persists to Chloranthaceae and into basal eudicots, but in the monocot-magnoliid clade ovule direction may either remain pendent or shift to ascendent. With the J/M tree, because Chloranthaceae and Ceratophyllum are nested in mesangiosperms, the pendent state unambiguously persists up to Acorus in the monocots. With both trees, a shift to the ascendent state occurs within Ranunculales (Menispermaceae, Berberi-daceae, and Ranunculaceae). The basic state in monocots other than Acorus is ascendent; this may be either ancestral for mono-cots (D & E) or derived from pendent (J/M). The ancestral state in magnoliids is entirely unresolved, but horizontal is basic in Pip-erales-Canellales and Magnoliales other than Myristicaceae (which have one basal, ascendent ovule). Ascendent is ancestral in Laurales, reverting to pendent in Gomortega and in the clade consisting of Monimiaceae, Lauraceae, and Hernandiaceae.

Inferences on the ancestral ovule curvature ( 93 ) depend on interpretation of Amborella , described as anatropous by Bai-ley and Swamy (1948) , orthotropous by Endress and Iger-sheim (2000b) and Yamada et al. (2001) , and hemianatropous (= hemitropous) by Tobe et al. (2000) . Based on the illustra-tions of both Endress and Igersheim (2000b) and Tobe et al. (2000) , the funicle is attached to one side of the base of the ovule, not halfway along the side of the ovule, as in the typical hemitropous condition. The asymmetry of the ovule base may be a consequence of the “ apical ” position of the ovule, which is actually attached to the adaxial cross zone; in our experi-ence, a truly symmetrical base is restricted to taxa with either basal ovules or apical ovules in a spacious locule (e.g., Acorus ; Buzgo and Endress, 2000 ). Because the Amborella condition seems closer to typical orthotropous than to anatropous, we have included it in the orthotropous state. With this scoring, the ancestral ovule curvature is equivocal if Amborella is sis-ter to all other angiosperms. However, the fact that the outer integument is asymmetric during development in both Ambo-rella and Chloranthus ( Yamada et al., 2001 ) suggests that orthotropous was derived from anatropous ( Endress and Igersheim, 2000b ). This is the most parsimonious hypothesis if Amborella and Nymphaeales form a clade. It is also favored if the bitegmic ovule is homologous with the cupule of Cayto-nia ( Gaussen, 1946 ; Stebbins, 1974 ; Doyle, 1978 ), as indi-cated by some cladistic analyses of seed plants ( Crane, 1985 ; Doyle and Donoghue, 1986 ; Doyle, 2006 , 2008; Hilton and Bateman, 2006 ). Orthotropous ovules evolved several other times, sometimes uniting clades: in Barclaya (Nymphae-aceae), Chloranthaceae and Ceratophyllum (a clade in D & E trees), Piperaceae and Saururaceae, Gomortega , Acorus , Cir-caeaster , and the Platanus -Proteaceae clade.

Summary of character discussion — Our results ( Table 1 ) imply that the ancestral angiosperm fl ower had more than two whorls (or series) of tepals, more than two whorls (series) of stamens, probably with adaxial microsporangia (introrse), and several ascidiate carpels that were sealed by secretion rather than postgenital fusion, most likely with one pendent bitegmic ovule, which was probably anatropous. These fl owers were

( Endress, 2001 ) are found in Amborella , Nymphaeales (except Nuphar ), and sometimes Trimenia and may be ancestral in an-giosperms. Abaxial nectaries ( 88 ) on the backs of the carpels are a synapomorphy of Buxaceae and Trochodendraceae. A widespread feature in monocots is septal nectaries ( 89 ) be-tween the fused carpels, seen in our data set in Dioscoreaceae and some Nartheciaceae. It has been suggested that lateral nec-taries on the free carpels of some Alismatales (represented by Tofi eldiaceae and Butomus ) may be homologous ( Daumann, 1970 ; Igersheim et al., 2001 ), and we scored them as the same state, but they originate independently on the trees.

Consideration of the last two characters and others treated earlier indicates that nectaries originated twice on the adaxial side of the inner perianth parts (37), in Cabomba and Ranuncu-lales; once or twice on the stamen bases (49) in Laurales; once on the backs of the carpels (88) within eudicots; and two or more times on the sides of the carpels (89) in monocots. Other types that we did not include because they differ morphologi-cally and appear to be autapomorphic are abaxial nectaries on the petals of Nuphar ( Hiepko, 1965 ; Endress, 2008a) and disc-like nectaries of uncertain morphological nature in Proteaceae ( Douglas, 1995 ) and Sabiaceae (not included in this data set; Ronse De Craene and Wanntorp, 2008 ). These results imply that nectar secretion itself arose independently at these different sites: even if all cases of nectar secretion were treated as a state of one character, none of the different types of nectaries would be inferred to be homologous.

In our previous analysis ( Doyle and Endress, 2000 ), the an-cestral ovule number ( 90 ) was equivocal: either one, as in Am-borella , Trimenia , Illicium , and Chloranthaceae, or more than two, as in most core Nymphaeales and Austrobaileya . Now, be-cause of the addition of Hydatellaceae, which are uniovulate, our data imply that one ovule is ancestral when only Recent taxa are considered ( Fig. 11A ) and that this number was re-tained up to Trimenia and Illicium in the Austrobaileyales and to Chloranthaceae (plus Ceratophyllum in D & E trees). How-ever, if Archaefructus , which has several ovules per carpel, is linked with Hydatellaceae, the ancestral state is still equivocal ( Fig. 11B ). Scenarios in mesangiosperms vary with the back-bone tree. With the D & E trees ( Fig. 11 ), where Ceratophyllum and Chloranthaceae form a clade at the base of the mesangio-sperms, the basic ovule number in the remaining mesangio-sperms is entirely equivocal, and the uniovulate condition in magnoliid groups such as Myristicaceae, Galbulimima , and Laurales (other than Calycanthaceae, which have two ovules) may be either a retention from the fi rst angiosperms or the result of reduction. However, the basic number in the Piperales-Canellales clade and in monocots is more than two, and the basic number in eudicots is either two or more. In contrast, with the J/M backbone, where Ceratophyllum and Chloranthaceae are nested at different points within the mesangiosperms, the uniovulate condition is retained from the base of the angio-sperms to these groups (unless Archaefructus is included, in which case the uniovulate condition in Ceratophyllum may be either primitive or secondary) and into Magnoliales and Lau-rales. This scenario would imply there were increases in ovule number in the Piperales-Canellales clade, Magnoliaceae, the Galbulimima -Annonaceae clade, Calycanthaceae, monocots, and eudicots. Secondary reduction to one ovule occurred in Piperaceae and Nelumbo .

Laminar placentation ( 91 ; including “ dorsal ” in Brasenia , actually on the carpel midrib), often noted as a similarity of Nymphaeales and Alismatales, was independently derived from


Fig. 10. (A) D & E tree, showing inferred evolution of an extragynoecial compitum (character 83). (B) Inferred evolution of carpel fusion (syncarpy; character 84). Abbreviations as in Fig. 2 .


borne either in racemes (which some authors might call shoots with axillary solitary fl owers) or in botryoids. Perianth and an-droecium phyllotaxis is uncertain, but if parts were whorled they were trimerous. The most striking uncertainty is whether the ancestral fl ower was bisexual or unisexual. This is an area where comparative studies on the genetic control of develop-ment and better understanding of fossil diversity could be most interesting. The clearest effect of considering Archaefructus concerns ovule number — whereas analysis of Recent taxa alone implies that one ovule was ancestral, the ancestral state be-comes ambiguous (either one or more than two) if Archaefruc-tus is linked with Hydatellaceae.

The “ explosive ” radiation of angiosperms appears to have begun with the origin of the mesangiosperm clade, after the ori-gin of crown group angiosperms and divergence of the more basal ANITA lines (cf. Moore et al., 2007 ). It should be noted that the beginning of this radiation, corresponding to the initial splitting of the main mesangiosperm lines, must have predated the radiation of angiosperms observed in the latter half of the Early Cretaceous fossil record (Barremian through Albian), which involved diversifi cation within the magnoliid, eudicot, and monocot clades ( Doyle and Hickey, 1976 ; Hughes, 1994 ; Doyle, 2001 ; Friis et al., 2006 ; Doyle and Endress, 2007 ). There is no unequivocal fl oral synapomorphy at this point in the tree that might be interpreted as a key innovation responsible for this radiation (cf. Cantino et al., 2007 ). Most mesangiosperms differ from the more basal lines in having plicate rather than ascidiate carpels, sealed by postgenital fusion rather than secre-tion. However, Chloranthaceae have ascidiate carpels that are notably similar to those of more basal groups ( Endress, 1987b , 2001 ; Endress and Igersheim, 2000a ). If the Doyle and Endress (2000) arrangement based on combined molecular and morpho-logical data is correct and Chloranthaceae (with or without Ceratophyllum ) are basal in mesangiosperms, plicate carpels originated at the next node; if Chloranthaceae are nested within mesangiosperms ( Jansen et al., 2007 ; Moore et al., 2007 ), pli-cate carpels may have originated either at the base of mesangio-sperms (but soon reversed) or several times within the clade. Furthermore, the fact that Chloranthaceae are one of the most prominent recognizable groups in the Early Cretaceous fossil record ( Friis et al., 1994 , 2006 ; Eklund et al., 2004 ; Feild et al., 2004 ) suggests they were part of any accelerated radiation. An apomorphy more closely tied to the base of the mesangiosperms is origin of the typical eight-nucleate female gametophyte and resultant formation of triploid rather than diploid endosperm ( Friedman and Williams, 2003 , 2004 ; Friedman, 2008 ; Rudall et al., 2008 ), but the history of this character is ambiguous be-cause Amborella has a nine-nucleate female gametophyte ( Friedman, 2006 ).

The fact that molecular data fi rmly nest Magnoliidae (in the restricted monophyletic sense of Cantino et al., 2007 ) well within the angiosperms calls into question the traditional use of magnoliid groups such as Magnoliales and Winteraceae as models for the original angiosperm fl ower (e.g., Cronquist, 1968 ; Takhtajan, 1969 ). However, fl owers of these groups are more like our present reconstruction of the ancestral fl ower than some that were being discussed before the molecular rooting — e.g., the simple fl owers of Chloranthaceae, suggested as one of several alternative prototypes by Endress (1986a) and found to be basal in some morphological cladistic analyses ( Nixon et al., 1994 ; Hickey and Taylor, 1996 ). According to our analysis, many putatively “ primitive ” magnoliid features were indeed retained from the fi rst angiosperms, such as more than two

whorls (or series) of perianth parts, several free carpels, and probably bisexuality. However, possession of more than two whorls (or series) of stamens may be a secondary increase from an intermediate stage with two whorls near the base of the me-sangiosperms. The laminar form of many magnoliid stamens may also be a reversal from more fi lamentous stamens in earlier mesangiosperms, and the abaxial position of the microsporan-gia in many magnoliids, which may refl ect this secondary ex-pansion, is more defi nitely derived. Whether the fi rst angiosperms had spiral or whorled fl oral phyllotaxis, the spiral perianth of some magnoliids appears to be derived from a whorled perianth lower in the mesangiosperms, and the same may be true for the androecium. Most notably, the plicate car-pels often illustrated in textbooks as primitive are instead de-rived, as is the elongate “ strobilar ” receptacle of Magnoliaceae. Evidence is also strong that the solitary fl owers of many mag-noliids are derived. Many of these derived features may be re-lated to a general increase in fl ower size and specialization for beetle pollination, like the inner staminodes of many Magno-liales and Laurales.

Floral groundplan of simple fl oral structure in near-basal angiosperms — The drastically simple reproductive structures of several extant basal angiosperms and Early Cretaceous fos-sils have provoked much recent discusion. In Ceratophyllum , fl owers are unisexual; female fl owers are unicarpellate, with an ascidiate carpel. The structures commonly interpreted as multi-staminate male fl owers ( Endress, 1994b ; Iwamoto et al., 2003 ) are more likely infl orescences of unistaminate fl owers without subtending bracts ( Endress, 2004 ), as we argued earlier. This interpretation becomes even more plausible if a relationship of Ceratophyllum and Chloranthaceae is envisaged ( Duvall et al., 2006 ; Mathews, 2006 ; Qiu et al., 2006 ), as supported by our analysis. The male structures of Hedyosmum are also infl ores-cences of unistaminate, perianthless fl owers without subtend-ing bracts ( Endress, 1987a ). Although Leroy (1983) interpreted these male shoots as fl owers, the infl orescence interpretation is more plausible based on comparison with male infl orescences in Ascarina , in which each stamen (or two to three stamens) is (are) subtended by a small subtending bract. Male shoots simi-lar to those in Hedyosmum are also known from the Early Cre-taceous ( Friis et al., 1994 , 2006 ).

Hydatellaceae and Archaefructus ( Sun et al., 2002 ) exhibit a similar pattern of very simple fl owers. In Hydatellaceae, sev-eral stamens are commonly surrounded by a number of ascidi-ate carpels, and these by two or more bracts ( Rudall et al., 2007 ). The simplest interpretation is that the fl owers are uni-sexual, unicarpellate or unistaminate, and perianthless ( Hamann, 1975 , 1976 , 1998 ; Rudall et al., 2007 ). In Archae-fructus , we interpret the fl owers as unisexual, 1 – 2-carpellate or usually 2-staminate, and perianthless ( Friis et al., 2003 ). Some authors have suggested that such structures may represent a prefl oral state ( Sun et al., 2002 ; Friis and Crane, 2007 ) or may be a result of secondary dissolution of the fl ower – infl orescence boundary due to loss of fl oral identity ( Rudall et al., 2007 ). Sun et al. (2002) speculated that the fertile structures of Archaefruc-tus might represent an evolutionary stage at which the genetic programs for fl ower and infl orescence formation were not yet strictly separated.

Our inferences on infl orescence, perianth, and androecium evolution do not support the suggestion that these taxa represent a prefl oral state. Although developmental studies show that a perianth is completely missing in Hydatellaceae, Ceratophyl-


Fig. 11. (A) D & E tree, showing inferred evolution of number of ovules per carpel (character 90). (B) D & E tree after addition of Archaefructus , show-ing different reconstruction of evolution of same character. Hernandioideae and Gyrocarpoideae combined as Hernandiaceae. Abbreviations as in Fig. 2 .


lum , and most Chloranthaceae (except female fl owers of Hedyos-mum ), and not even present as rudiments in early developmental stages ( Endress, 1987b , 1994b ; Kong et al., 2002 ; Iwamoto et al., 2003 ; Rudall et al., 2007 ), our results imply that the simple fl oral structure of these groups and Archaefructus is a result of reduction (i.e., decrease in organ number, loss of a perianth, and probably loss of bisexuality) of more “ complete ” ancestral fl ow-ers with a perianth and several stamens and carpels. On parsi-mony grounds, it is equivocal whether the ancestral fl ower was bisexual, but we suspect it was, for the reasons discussed.

On phylogenetic grounds, it is less easy to eliminate the hy-pothesis that fl oral reduction in these groups occurred not by gradual loss of parts but by loss of fl oral identity, one of three possibilities discussed by Rudall et al. (2007) . However, if Ar-chaefructus is related to either Hydatellaceae or Ceratophyl-lum , the fact that its fl owers had usually two stamens and one or two carpels may support a reduction scenario. Loss of fl oral organs may have been easier in more basal angiosperms be-cause they had less fl oral synorganization than more derived clades. However, we see no reason to think that this involved loss of the basic fl oral program. A more conservative hypothe-sis is that the basic fl oral program was still present but the fl ow-ers became simpler by loss and reduction of organs, and selection for maintenance of suffi cient reproductive output favored production of more fl owers per individual or per infl orescence.

This view is supported by recent molecular developmental studies on Amborella and Nymphaeales, which suggest that the fl oral genetic program originally found in Arabidopsis and An-tirrhinum ( Coen and Meyerowitz, 1991 ) is present with similar function in these basalmost extant angiosperm lines. Further-more, the program does not differ profoundly between Ambo-rella and Nymphaeales, in which Nuphar has been studied ( Soltis et al., 2006 ). The same is true for Illicium , another mem-ber of the ANITA grade, and some magnoliids ( Asimina , Eupo-matia , Liriodendron , Magnolia , Persea : Kim et al., 2005a , b ; Chanderbali et al., 2006 ; Soltis et al., 2006, 2007 ; Buzgo et al., 2007 ). In Chloranthus class A genes (responsible for perianth identity in Arabidopsis and Antirrhinum ) are present, although its fl owers do not have a perianth ( Li et al., 2005 ). It appears that one of the mechanisms for the early evolutionary modifi ca-tion and elaboration of the fl oral developmental program was repeated events of gene duplication and sub- or neofunctional-ization ( Irish and Litt, 2005 ; Zahn et al., 2005 ; Irish, 2006 ; Kramer and Zimmer, 2006 ). This is certainly a promising track to follow in evo-devo studies.

Extant angiosperms that fl ower under water and peculiari-ties of their reproductive structures — Because Hydatellaceae, Archaefructus , and Ceratophyllum are or were water plants, it is useful to consider if and how the scenarios developed here may be functionally related to a shift from a terrestrial to an aquatic habitat. For this purpose, we cursorily surveyed repro-ductive morphology in all angiosperm families comprising taxa with underwater fl owers. Comparisons with these taxa suggest that fl oral simplicity comparable to that in more basal aquatic groups has frequently arisen by reduction. We emphasize that we are not using these correlations as evidence for one or an-other concept of relationships or direction of evolution; rather, we present them as possible biological explanations for the changes inferred from phylogenetic trees. However, it would be fair to take functional correlations among reduced fl oral fea-tures as evidence that these characters have less individual

weight than many others and a reason to exercise caution in ac-cepting relationships based on them. Physical conditions are very different in the water and in the air, and the evolutionary transition from the air to the water has a profound impact on plant structure and fl ower biology ( Sculthorpe, 1967 ; Vogel, 1996 ; Voesenek et al., 2006 ). A morphological interpretation of submerged fl owers should take into account these differences.

Among angiosperms systematic surveys show many in-stances of evolution from the land to the water ( Cook, 1999 ), and shifts from pollination in the air to under the water (or on its surface) also occurred a number of times, whereas there are no clear reversals. Based on our survey, there is clearly a gen-eral tendency for underwater-fl owering plants to evolve simple, unisexual, perianthless, and unistaminate or unicarpellate fl ow-ers. This reduction trend is especially conspicuous in near-basal monocots (Alismatales), but it is also recognizable (usually in less extreme form) in other angiosperms. In Alismatales there is a broad diversity of plants with underwater fl owering, diverse modes of water-surface fl owering, and fl owering in the air. Phylogenetic analyses show that the taxa with submerged fl ow-ers are derived from taxa with aerial fl owers. That there is really an evolutionary trend is shown by the fact that underwater pol-lination did not evolve just once in Alismatales but several times ( Les et al., 1997 ; Chen et al., 2004 ).

Another possibility to consider is that the underwater-fl ow-ering habit may have often evolved from wind pollination. A number of water plants have emergent infl orescences and wind-pollinated fl owers ( Cook, 1988 ). Wind pollination and underwater pollination can lead to similar reductions in fl oral structure (see discussion in Endress, 1994a ). Thus features adapted to wind pollination may have been preadaptations for underwater pollination. This evolutionary pathway is consis-tent with the fact that there are genera in which wind pollina-tion and underwater pollination co-occur, such as Groenlandia (Potamogetonaceae) ( Guo and Cook, 1990 ) and Callitriche (Plantaginaceae) ( Philbrick and Les, 2000 ). However, in gen-eral, fl oral reduction is even stronger in water-pollinated than in wind-pollinated fl owers. This scenario is a real possibility for Ceratophyllum if it is related to Chloranthaceae, which ap-pear to be ancestrally wind-pollinated, as in Hedyosmum and Ascarina ( Endress, 1987b ).

In Alismatales, there are eight families in which some or all members have submerged fl owers (Cymodoceaceae, Hy-drocharitaceae, Juncaginaceae, Posidoniaceae, Potamoget-onaceae, Ruppiaceae, Zannichelliaceae, and Zosteraceae). These families are representatives of both major aquatic clades in the order ( Chase et al., 2006 ; Les et al., 2006 ). Of these eight families, fi ve have unisexual fl owers. Six have pe-rianthless fl owers, some with a spathe-like envelope (vs. two with a single whorl of perianth organs). It is uncertain whether this envelope is a modifi ed perianth or a bract. Five have uni-staminate or bistaminate male fl owers (vs. three with three or more stamens). Seven have at least partly unicarpellate or bi-carpellate female fl owers (vs. one with three or more carpels) ( Doty and Stone, 1966 ; Tomlinson, 1969 , 1982 ; Cook, 1998b ; Haynes et al., 1998a, b, e , g; Kuo and McComb, 1998a – c ; Igersheim et al., 2001 ).

In contrast, there are seven families in Alismatales without submerged fl owers (Alismataceae, Aponogetonaceae, Araceae, Butomaceae, Limnocharitaceae, Scheuchzeriaceae, Tofi el-diaceae). In all of these, the fl owers are either always or some-times bisexual. All have a perianth of two whorls, six or more stamens, and at least three carpels, except for derived groups of


Araceae ( Kaul, 1968 ; Cook, 1998a ; Haynes et al., 1998c , d, f ; Mayo et al., 1998 ; van Bruggen, 1998 ; Igersheim et al., 2001 ).

A family of Alismatales that particularly well illustrates the evolutionary fl exibility of fl owers is Juncaginaceae. It shows not only an evolutionary transition from aerial to submerged fl owers and correlated morphological changes but also conspicuous lability of fl ower forms in the group with submerged fl owers. Some Juncaginaceae have spikes of aerial fl owers (e.g., Tri-glochin ), which are trimerous and bisexual, with two whorls of tepals. Lilaea , however, is a submerged water plant, also with spikes. Phylogenetic analyses nest Lilaea within the family ( Les et al., 1997 ; Chen et al., 2004 ; von Mering and Kadereit, 2006 ), implying that its submerged habit is derived. There are fi ve dif-ferent fl oral morphs within one species, all very simple, includ-ing from the top downward in a spike ( Posluszny et al., 1986 ): (1) male fl owers, unistaminate, associated with a bract-like or-gan, which could be a fl oral subtending bract or a tepal (inter-preted as a tepal by Posluszny et al., 1986 ); (2) bisexual fl owers, unistaminate and with a single carpel, associated with a bract-like organ; (3) female fl owers of a single short-styled carpel, as-sociated with a bract-like organ; (4) female fl owers of one

short-styled carpel with no bract-like organ; and (5) female fl ow-ers of one very long-styled carpel with no bract-like organ. Whether the bract-like organ is a fl oral subtending bract or a pe-rianth part, the fl owers are extremely simple in terms of organ numbers.

Thus, although more surveys from a phylogenetic perspec-tive would be desirable, Alismatales can serve as a model group to show functional changes in reproductive structures correlated with the transition from aerial to submerged fl owers. Similar patterns can be seen in other groups with completely or partly submerged fl owers. In Lamiales, Callitriche (Plantaginaceae) has unisexual, perianthless fl owers, male fl owers unistaminate, female fl owers with two carpels; Hydrostachys (Hydrostachy-aceae) has unisexual, perianthless fl owers, male fl owers uni- or bistaminate, female fl owers with two carpels ( Erbar and Leins, 2003 , 2004 ). The two genera have the most reduced fl owers in Lamiales, which usually have bisexual fl owers with a perianth of two whorls and at least two stamens. In Malpighiales, some Podostemaceae have submerged (cleistogamous) fl owers, many perianthless and uni- or bistaminate ( Cook and Rutishauser, 2007 ); some species of Bergia and Elatine (Elatinaceae) have

Fig. 12. D & E tree, showing inferred evolution of ovule direction (character 92). Abbreviations as in Fig. 2.


position of Ceratophyllum underline the dangers of associating it with a particular extant group. More secure conclusions on its affi nities may require recognition of other fossils that link it with one rather than another living taxon. Whether Archaefructus affects ideas about the fi rst fl ower, it reveals important early trends in fl oral evolution and the early ecological radiation of angiosperms (cf. Feild et al., 2004 ). Especially if it is related to the Albian genera Vitiphyllum and Caspiocarpus ( Friis et al., 2003 ), which had similar but less fi nely dissected leaves, it rep-resents an important trend for invasion of Early Cretaceous aquatic ecosystems by angiosperms (cf. Mart í n-Closas, 2003 ), represented today only by Hydatellaceae, core Nymphaeales, and probably Ceratophyllum .

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Groups with submerged fl owers often have bracts below the whole infl orescence, even when they lack fl oral subtending bracts, as in Hydatellaceae and some Alismatales. The apparent absence of infl orescence bracts in Archaefructus ( Sun et al., 2002 ; Friis et al., 2003 ) might be considered evidence against the hypothesis that it was adapted to an underwater fl owering habit. However, when there are no fl oral subtending bracts that individually protect youngest fl oral stages, infl orescences may have some protection by more basal leaves. In Archaefructus , infl orescences were enclosed by leaves in bud, as shown in the type specimen of A. eofl ora (Figs. 2, 26 in Ji et al., 2004 ), which has younger stages of reproductive parts than A. sinensis in Sun et al. (2002) . In Cabombaceae, young infl orescences are en-closed by regular leaves below the infl orescence and fl oral sub-tending leaves, and the same is true of some Alismatales. In the nonaquatic family Chloranthaceae, the infl orescences are en-closed in early development by the fused stipules of adjacent leaf pairs, which form a sheathing structure. In many species of Hedyosmum , the unistaminate male fl owers, which lack a sub-tending bract, are protected by a massive sterile apical part ( En-dress, 1987b , 2008b ).

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Taxa

1. Amborella (= Amborellaceae).

2. * Cabomba (Cabombaceae).

3. * Brasenia (Cabombaceae).

4 – 6. Nymphaeaceae ( Ito, 1987 ; Les et al., 1999 ; Schneider et al., 2003 ).

4. Nuphar.

5. Barclaya ( Williamson and Schneider, 1994 ).

6. Nymphaeoideae (= Nymphaea s. lat.). Ondinea , Euryale , and Victoria assumed to be nested within Nymphaea ( L ö hne et al., 2007 ).

7. *Hydatellaceae ( Hamann, 1975 , 1976 ; Rudall et al., 2007 , 2008 ; Friedman, 2008 ).

8. Austrobaileya (= Austrobaileyaceae).

9. Trimenia (= Trimeniaceae, including Piptocalyx ).

10. Illicium (= Illiciaceae) ( Oh et al., 2003 ).

11. Schisandraceae ( Saunders, 1998 , 2000 ; Liu et al., 2006 ).

12 – 15. Chloranthaceae: Endress (1987b) , Zhang and Renner (2003) , Eklund et al. (2004) .

12. Hedyosmum . Subgenus Tafalla (with fused fl oral bracts) assumed to be a derived subgroup.

13. Ascarina .

14. * Sarcandra .

15. * Chloranthus .

16. * Liriodendron (Magnoliaceae).

17. *Magnolioideae (= Magnolia s.l., Magnoliaceae). Rooting uncertain, but analyses agree that Aromadendron , Alcimandra , Manglietia , and Michelia are nested ( Azuma et al., 2001 ; Kim et al., 2001 ).

18. Degeneria (= Degeneriaceae).

19. Galbulimima (= Himantandraceae).

20. Eupomatia (= Eupomatiaceae).

21. Annonaceae. Anaxagorea is assumed to be basal and the ambavioid clade (including Cananga ) sister to the remaining clades ( Doyle and Le Thomas, 1996 ; Doyle et al., 2000 ; Richardson et al., 2004 ).

Appendix 1. Taxa, characters, and sources of data In the taxon list, we indicate taxa added or subdivided since Doyle and Endress (2000) with an asterisk. We cite here phylogenetic studies on internal relationships

that we consulted to estimate ancestral states in characters that vary within the group.In the character list, DE designates character numbers in Doyle and Endress (2000) . When not otherwise indicated, scorings of taxa follow Doyle and Endress (2000)

and are based on references cited therein, including most generally Cronquist (1981) and Kubitzki (1993 , 1998 ). Sources of data for taxa added or subdivided since Doyle and Endress (2000) are listed either in the taxon list when they are focused on specifi c taxa or under individual characters or groups of characters when they survey characters across many taxa, as most convenient.

The data matrix is presented as Table 2 .


50. Nelumbo (= Nelumbonaceae).

51. Platanus (= Platanaceae, not including putative Cretaceous relatives).

52. Proteaceae. Scoring based primarily on Bellendena and Persoonioideae, which form either two basal lines or a clade ( Hoot and Douglas, 1998 ; Jordan et al., 2005 ).

53. * Tetracentron (Trochodendraceae).

54. * Trochodendron (Trochodendraceae).

55. Buxaceae (not including putative Cretaceous relatives). Buxus (including Notobuxus ) assumed to be sister to the remaining taxa, Sarcococca basal in the rest ( von Balthazar et al., 2000 , 2002b).

56. Acorus (= Acoraceae).

57. Tofi eldiaceae ( Zomlefer, 1997c ).

58. Butomus (= Butomaceae).

59. * Aponogeton (= Aponogetonaceae) ( van Bruggen, 1998 ).

60. * Scheuchzeria (= Scheuchzeriaceae).

61. Araceae. Based primarily on Gymnostachys , Pothos , Lysichiton , and Orontium ( French et al., 1995 ).

62. *Nartheciaceae. Zomlefer (1997b) ; basal split assumed to be between Narthecium - Lophiola and Aletris - Metanarthecium ( Caddick et al., 2002a ).

63. Dioscoreaceae. Stenomeris , Tacca , and Trichopus plus Dioscorea treated as forming a trichotomy ( Caddick et al., 2002b ).

64. *Melanthiaceae. Schulze (1978), Zomlefer (1997a) ; assumed internal relationships as in Zomlefer et al. (2001) .

65. * Ceratophyllum (= Ceratophyllaceae). Rutishauser and Sattler (1987) , Endress (1994b) , Iwamoto et al. (2003) .

66. * Archaefructus inf: fertile axis interpreted as an infl orescence. See text for references and discussion of scoring.

67. * Archaefructus fl o: fertile axis interpreted as a (pre)fl ower.

68. * Archaefructus NP: same as Archaefructus inf but with pollen characters (59-73) removed.

Characters

1 (DE 1). Habit (0) tree or shrub, (1) rhizomatous, scandent, or acaulescent. Amborella rescored as (1) based on seedling establishment pattern described by Feild et al. (2001) . Berberidaceae rescored as (1) based on revised internal relationships.

Anatomical characters (2 – 4, 6 – 8, 14 – 15, 21): references in Doyle and Endress (2000) , especially Metcalfe and Chalk (1950) and Metcalfe (1987) ; Hydatellaceae: Cutler (1969) ; added monocots: Buxbaum (1922 , 1927 ), Tomlinson (1982) ; Ceratophyllum : Ito (1987) , Schneider and Carlquist (1996) .

2 (DE 4). Protoxylem lacunae (0) absent, (1) present.

3 (DE 14). Pith (0) uniform, (1) septate (plates of sclerenchyma). Chloranthaceae changed from (?) to (0) based on anatomical collections at Harvard and Kew (JAD); Myristicaceae from (0) to (1), Hernandioideae from (?) to (0) based on Sauquet et al. (2003) .

4 (DE 5). Cambium (0) present, (1) absent. Circaeaster : Foster (1963) .

5 (DE 16). Sieve tube plastids (0) S-type (starch), (1) PI-type, (2) PII-type. Behnke (1981 , 1988 , 1995 , 2000 ).

6 (DE 17 part). Fibers or sclerenchyma in pericyclic area (including modifi ed protophloem) of vascular bundles (0) present, (1) absent.

7 (DE 18). Laticifers in stem (0) absent, (1) present.

8 (DE 19). Raphide idioblasts (0) absent, (1) present. Prychid and Rudall (1999) .

9 (DE 20 part). Phyllotaxis (0) alternate (spiral or distichous), (1) opposite or whorled.

22. Myristicaceae. Scoring modifi ed based on Sauquet et al. (2003) , who showed that the basal split is not between Mauloutchia and rest of the family, as assumed by Doyle and Endress (2000) , but rather between the myristicoid and combined pycnanthoid-mauloutchioid clades.

23. Calycanthoideae (Calycanthaceae). Following APG (2003) and Staedler et al. (2007) , we include Idiospermum in Calycanthaceae and designate the remaining genera as Calycanthoideae. Chimonanthus assumed to be sister to other Calycanthoideae ( Li et al., 2004 ).

24. Idiospermum .

25. Atherospermataceae. Daphnandra and Doryphora assumed to be sister to the rest of the family, Atherosperma well nested ( Renner et al., 2000 ).

26. Siparunaceae. Glossocalyx and Siparuna assumed to be sister groups (Renner, 1998).

27 – 29. Monimiaceae: internal relationships based on Renner (1998).

27. Hortonia .

28. Monimioideae. Peumus assumed to be sister to Monimia and Palmeria (Renner, 1998, 2004 ).

29. Mollinedioideae. Hedycarya and Xymalos assumed to be relatively basal (Renner, 1998, 2004).

30. Gomortega (= Gomortegaceae).

31. Lauraceae. Hypodaphis assumed to be basal, next the cryptocaryoid clade ( Rohwer and Rudolph, 2005 ).

32 – 33. Hernandiaceae ( Kubitzki, 1969 ).

32. *Hernandioideae ( Hernandia and Illigera ).

33. *Gyrocarpoideae ( Gyrocarpus and Sparattanthelium ).

34. Winteraceae. Takhtajania assumed to be sister to the rest of the family, Tasmannia basal in the rest ( Karol et al., 2000 ).

35. Canellaceae. Rooting uncertain, but Capsicodendron and Cinnamosma assumed to be well nested ( Karol et al., 2000 ).

36. Saururaceae. Basal split not between Saururus and the remaining genera but between Saururus - Gymnostachys and Anemopsis - Houttuynia ( Meng et al., 2002 , 2003 ).

37. Piperaceae. Zippelia and Manekia (= Sarcorhachis ) assumed to be basal, not Zippelia alone ( Jaramillo et al., 2004 ).

38. Lactoris (= Lactoridaceae).

39. Asaroideae (Aristolochiaceae).

40. Aristolochioideae (Aristolochiaceae). Thottea assumed to be basal ( Neinhuis et al., 2005 ).

41. Euptelea (= Eupteleaceae).

42. Papaveraceae (= Papaverales in Doyle and Endress, 2000 ). Pteridophyllum , then Hypecoum plus Fumarioideae assumed to be second and fi rst outgroups to the remaining Papaveraceae ( Hoot et al., 1997 ).

43. Lardizabalaceae. Sargentodoxa , Decaisnea , and Sinofranchetia in that order assumed to be basal to the remaining genera ( Hoot et al., 1995 ; Wang et al., 2002 ).

44. * Circaeaster (Circaeasteraceae). Hu and Yang (1987) , Hu et al. (1990) .

45. Menispermaceae.

46. Berberidaceae. Nandina assumed to be linked with Caulophyllum , Gymnospermium , and Leontice rather than basal (Kim et al., 2004; Wang et al., 2007 ).

47 – 49. Ranunculaceae: Glaucidium and Hydrastis assumed to be sister to the rest of the family, within which Xanthorhiza and Coptis are basal ( Hoot, 1995 ).

47. * Glaucidium ( Tamura, 1972 ; Tobe and Keating, 1985 ).

48. * Hydrastis ( Tobe and Keating, 1985 ).

49. *Core Ranunculaceae.


10 (DE 20 part). Distichous phyllotaxis (0) absent, (1) on some or all branches. Characters 9 and 10: spiral in Hydatellaceae confi rmed by Rudall et al. (2007) ; Cabombaceae: Chassat (1962) , Richardson (1969) , Moseley et al. (1984) , Rutishauser and Sattler (1987) ; monocots: see general references; Circaeaster : spiral based on fi gures in Foster (1968) ; Glaucidium , Hydrastis : Tobe and Keating (1985) ; Proteaceae: changed from spiral/distichous to spiral based on basal groups (our observations); Tetracentron : our observations; Ceratophyllum : Rutishauser and Sattler (1987) speculated that the whorled leaves were derived by fragmentation of a single leaf, but they and Les (1985) showed that phyllotaxis is initially decussate in the seedling.

11 (DE 22 modifi ed). First appendage(s) on vegetative branch (0) paired lateral prophylls, (1) single distinct prophyll (adaxial, oblique, or lateral). State labeling inadvertently reversed in Doyle and Endress (2000) due to an editing error. Changes in scoring: Cabomba from (?) to (0), Nuphar and Nymphaeoideae from (0) to (1) ( Chassat, 1962 ); Degeneria from (?) to (1), Siparunaceae from (?) to (0) ( Sauquet et al., 2003 ); Trimenia and Ascarina from (?) to (0) ( Eklund et al., 2004 ). Platanus , mistakenly scored (0) by Doyle and Endress (2000) although we cited Henry (1847) for one large lateral prophyll, is rescored as (1). Hydatellaceae: based on lateral prophylls in the reproductive units ( Rudall et al., 2007 ). Ceratophyllum : Rutishauser and Sattler (1987) .

12 (new). Leaf base (0) nonsheathing, (1) sheathing (half or more of stem circumference). General references on taxa and our observations.

13 (DE 23 modifi ed). Stipules (0) absent, (1) adaxial/axillary, (2) interpetiolar, (3) paired cap. State (3), in Magnoliaceae, previously omitted as autapomorphic and uninformative, is added because Magnoliaceae have been split into two taxa. Acorus and Tofi eldiaceae changed from (1) to (0): the “ stipules ” are not more developed than fl anges of the leaf sheath in other monocots (cf. Bharathan, 1996 ).

14 (DE 24). Axillary squamules (0) absent, (1) present. Hydatellaceae: long trichomes near the axils but not scales ( Rudall et al., 2007 ).

15 (DE 25). Leaf blade (0) bifacial, (1) unifacial. Hydatellaceae scored as bifacial based on the triangular shape of primordia ( Rudall et al., 2007 ). Added monocots: Zomlefer (1997b) , Rudall and Buzgo (2002) .

Leaf architectural characters (16 – 20): general references, Doyle (2007) , and our observations. Hydatellaceae and Ceratophyllum scored as unknown for some characters because of extreme simplicity and incomparability with ordinary leaves.

16 (DE 26). Leaf shape (0) obovate to elliptical to oblong, (1) ovate, (2) linear. Trimenia changed from (0) to (0/1) because species formerly placed in Piptocalyx are ovate ( Eklund et al., 2004 ); Euptelea changed from (0) to (0/1) following Doyle (2007) .

17 (DE 27 modifi ed). Major venation (0) pinnate with secondaries at more or less constant angle, (1) palmate (actinodromous or acrodromous) or crowded (pinnate with crowded basal secondaries, upward decreasing angle), (2) parallel (lateral veins departing at low angles from the midrib and converging and fusing apically). Parallel added as discussed in Doyle (2007) . Buxaceae changed from (0/1) to (1) based on presence of both states in Buxus and palmate in other genera.

18 (new). Fine venation (0) reticulate, (1) open dichotomous in some or all leaves. Defi nitions of characters 18 – 20 assume that the occurrence of the (1) state in some but not all leaves of an individual is potential evidence for relationship.

19 (DE 28 modifi ed). Base of blade (0) not peltate, (1) peltate in some or all leaves.

20 (DE 29 modifi ed). Leaf dissection (0) simple, (1) some or all leaves lobed or compound.

21 (DE 34). Asterosclerids in mesophyll (0) absent, (1) present.

Infl orescence characters (22 – 25): references in Doyle and Endress (2000) , particularly Weberling (1988) ; references cited in text for Nymphaeales, Chloranthaceae, and Ceratophyllum ; and general references on added taxa. See text for discussion. When male and female infl orescences differ, we base scoring on the type with more complex structure. Variation in Schisandraceae: Weberling (1988) , Saunders (1998 , 2000 ); Lactoris described by Gonz á lez and Rudall (2001) as having

cymes (rhipidia), but our observations indicate they have botryoids (1); Aristolochioideae: thyrses inferred to be ancestral ( Gonz á lez, 1999 ); Myristicaceae: De Wilde (1991) ; Annonaceae: rhipidia appear to be ancestral ( Doyle and Le Thomas, 1996 ; Richardson et al., 2004 ), most comparable with thyrsoids; Laurales: Endress and Lorence (personal observations); monocots: Markgraf (1981) , Posluszny (1983) , and Remizova and Sokoloff (2003) as well as references listed for taxa; Circaeaster : thyrsoid ( Tian et al., 2006 ); Nelumbo : special raceme based on Chassat (1962) and Esau and Kosakai (1975) ; Buxaceae: von Balthazar and Endress (2002a).

22 (DE 37 part). Infl orescence (0) solitary fl ower (or occasionally with 1 – 2 lateral fl owers), (1) botryoid, panicle, or thyrsoid (monotelic), (2) raceme, spike, or thyrse (polytelic).

23 (new). Infl orescence partial units (0) single fl owers, (1) cymes.

24 (new). Pedicel (0) present in some or all fl owers, (1) absent or highly reduced (fl ower sessile or subsessile). Saururaceae: Tucker et al. (1993) scored Saururus and Gymnotheca as pedicellate, but Gymnotheca ( Liang, 1994 ) is subsessile as defi ned here; Piperaceae: Zippelia has a short pedicel ( Liang and Tucker, 1995 ), but Manekia is sessile ( Steyermark, 1971 ), and pedicellate species of Piper are deeply nested ( Jaramillo and Manos, 2001 ); Buxaceae: von Balthazar and Endress (2002a, b).

25 (new). Floral subtending bracts (0) present, (1) present in female, absent in male fl owers, (2) absent in all fl owers.

For old and new characters of fl oral organization (26 – 47), we consulted references in Doyle and Endress (2000) and Ronse De Craene et al. (2003) .

26 (DE 38 modifi ed). Sex of fl owers (0) bisexual, (1) unisexual. State (1) covers both structural and functional unisexuality. Taxa scored as having the former bisexual and unisexual state are rescored as (0/1), since this state was found only in Trimenia and Lactoris and dissimilar in these, or mixed with unisexual in Lardizabalaceae. Winteraceae changed from (0/1) to (0) based on the basal position of Takhtajania . Lardizabalaceae changed to unisexual based on relationships assumed here and the fi nding that pollen in apparent bisexual fl owers of Decaisnea and Sinofranchetia is abortive ( Qin, 1997 ).

27 (DE 39 modifi ed). Floral base (0) hypanthium absent, superior ovary, (1) hypanthium present, superior ovary, (2) partially or completely inferior ovary. Saururaceae: changed from (0) to (2) based on evidence Saururus is nested; Melanthiaceae: relationships and data of Zomlefer et al. (2001) imply superior is ancestral; Trochodendraceae: changed from (0/2) to (2) because both tepals and stamens are fused to the ovary in Tetracentron , and although Trochodendron lacks a perianth, its stamens show similar fusion ( Endress, 1986b ).

28 (new). Floral receptacle (female portion) (0) short, (1) elongate. Cases of elongate receptacle in Annonaceae appear to be derived ( Doyle and Le Thomas, 1996 ).

29 (new). Cortical vascular system (0) absent or supplying perianth only, (1) supplying androecium, (2) supplying androecium plus gynoecium. Data from Ronse De Craene et al. (2003) . Annonaceae scored (0/1) based on absence in Anaxagorea and presence in Cananga ( Deroin, 1991 ).

30 (new). Floral apex (0) used up after production of carpels, (1) protruding in mature fl ower. Unicarpellate taxa scored as unknown.

31 (DE 41 part). Perianth (0) present, (1) absent. See text for discussion. Eupomatia changed from one cycle (DE 41) to absent, based on evidence that the calyptra is a bract ( Endress, 2003 ; Kim et al., 2005a); Galbulimima from one to unknown, because the two calyptrate outer organs appear to be bracts ( Endress, 1977 , 2003 ), but the petaloid parts might be either outer staminodes or tepals; Trochodendron scored as unknown, since it is unclear whether the small nubs below the stamens ( Endress, 1986b ; Wu et al., 2007 ) are tepals, staminodes, or bracts.

32 (DE 40). Perianth phyllotaxis (0) spiral, (1) whorled. See Endress and Doyle (2007) . Barclaya : Williamson and Schneider (1994) ; Atherospermataceae from (0/1) to spiral, because the whorled genus Dryadodaphne is nested ( Renner et al., 2000 ); Siparunaceae and Monimioideae rescored as unknown because perianth is too reduced to interpret; core Ranunculaceae scored as spiral based on data of Sch ö ffel (1932) , Hiepko (1965) , Endress (1995) , and Tamura (1995) in the context of the phylogeny of Hoot (1995) .


33 (DE 42 modifi ed). Perianth merism (0) trimerous, (1) dimerous, (2) polymerous. Spiral taxa scored as unknown. See text for discussion. Both Magnoliaceae (formerly irregular/trimerous) rescored as trimerous, since spiral taxa appear to be nested in Magnolioideae; Degeneria changed from trimerous to unknown because phyllotaxis is spiral; Hernandiaceae from both irregular to Hernandioideae (0/1/2), Gyrocarpoideae (2) based on variation in Kubitzki (1969) ; Hydrastis : Tamura (1995) ; Platanus from 2,4,5-parted to (0/2) because we have excluded the dimerous fossil Quadriplatanus (Magall ó n-Puebla et al., 1997) and have not resolved the confl icting observations of Sch ö nland (1883) and Bretzler (1924) .

34 (DE 41 modifi ed). Perianth whorls (series when phyllotaxis is spiral) (0) one, (1) two, (2) more than two. Includes petals (character 36); taxa with no perianth scored as unknown. Asaroideae changed from two to (0/1) because small “ petals ” in Asarum are not clearly equivalent to petals of Saruma and not known to be ancestral; Canellaceae from more than two to (1/2) based on data of Gilg (1925) and Wilson (1966) in the context of the phylogeny of Karol et al. (2000) ; Siparunaceae from one to (0/1), Monimioideae from more than two to (1/2), because of uncertain merism; Hernandioideae from two to (1/2) to allow interpretation of supposedly tetramerous fl owers as dimerous ( Kubitzki, 1969 ; Endress and Lorence, 2004 ); Ranunculaceae: see character 32; Platanus from two/one to (1/2): see character 33.

35 (DE 43 modifi ed). Tepal differentiation (0) all more or less sepaloid; (1) outer sepaloid, inner distinctly petaloid; (2) all distinctly petaloid. Does not include petals (36). Single sepaloid cycle scored as (0/1). Several taxa scored as uncertain to accommodate uncertain interpretations of whorl number.

36 (new). Petals (0) absent, (1) present. Petals as defi ned here usually have a narrow base and only one vascular trace, and although initiated acropetally, they usually lag behind sepals and stamens in development ( Hiepko, 1965 ). Cabomba scored as unknown because the inner organs are delayed but otherwise similar to the outer ( Endress, 2001 ), Brasenia not suffi ciently studied; Lardizabalaceae: lack of petals in Decaisnea and Akebia appears derived based on phylogenetic relationships; Glaucidium : showy parts are outermost and have several veins and thus not petals ( Hiepko, 1965 ).

37 (DE 45 modifi ed). Nectaries on inner perianth parts (0) absent, (1) present. Cabomba rescored as present: its nectaries are not small, isolated nectar-secreting areas like the nectarioles of Chimonanthus and Schisandraceae, with which we compared them in Doyle and Endress (2000) , but are two large areas that secrete nectar through special hairs ( Vogel, 1998 ; Endress, 2008a).

38 (DE 44 part). Outermost perianth parts (0) free, (1) at least basally fused. Amborella , Cabomba : Endress (2008a).

39 (DE 44 part). Calyptra derived from last one or two bracteate organs below the fl ower (0) absent, (1) present. Split from the previous character because it involves parts of apparently different homologies ( Endress, 1977 , 2003 ; Kim et al., 2005a).

40 (new). Stamen number (0) more than one, (1) one. See text for discussion.

41 (DE 46). Androecium phyllotaxis (0) spiral, (1) whorled. See Endress and Doyle (2007) . Irregular state of DE 46 eliminated: Annonaceae rescored as whorled, based on the outer stamens ( Endress, 1987a ; Erbar and Leins, 1994 ; Leins and Erbar, 1996 ), and Nelumbo , where stamens arise chaotically on a ring primordium ( Hayes et al., 2000 ), as unknown. Barclaya : Williamson and Schneider (1994) ; Myristicaceae scored (0/1) based not on spiral in Mauloutchia , which now appears derived ( Sauquet et al., 2003 ), but on possible spiral arrangement in early development of Myristica ( Armstrong and Tucker, 1986 ); Atherospermataceae: see character 32; Siparunaceae rescored as unknown because although Siparuna thecaphora (= andina ) is whorled ( Endress, 1980 ), this species is nested in the genus, and others are irregular ( Renner et al., 1997 ; Renner and Hausner, 2005 ); Hydrastis and Glaucidium not suffi ciently studied, possibly chaotic (?); core Ranunculaceae: see character 32; Trochodendron : spiral to approximately whorled ( Endress, 1990 ).

42 (DE 47 modifi ed). Androecium merism (0) trimerous, (1) dimerous, (2) polymerous. Spiral taxa scored as unknown. See text for discussion. Nymphaeaceae changed from irregular to polymerous ( Endress, 2001 ); Piperaceae changed from trimerous to (0/1) based on Jaramillo et al. (2004) ; Winteraceae from irregular to polymerous ( Doust, 2001 );

Canellaceae from irregular/trimerous to polymerous ( Wilson, 1966 ; Occhioni, 1994 ); Myristicaceae from irregular to trimerous, which is most likely to be ancestral in the family if the original phyllotaxis was whorled (Sauquet, 2003); Annonaceae from irregular to trimerous (references for character 41); Hernandiaceae from irregular to polymerous based on Kubitzki (1969) ; Trochodendron has several stamens per whorl if it is whorled ( Endress, 1990 ).

43 (new). Number of stamen whorls (series when phyllotaxis is spiral; includes inner staminodes) (0) one, (1) two, (2) more than two. Single stamens scored as unknown to avoid redundancy with character 40. See general references and those for characters 41, 42, and 44. Illicium : reconstructed ancestral number 11 – 30 ( Oh et al., 2003 ) could represent either (1) or (2); Saururaceae: one whorl in Houttuynia appears to be derived ( Meng et al., 2002 , 2003 ); Euptelea : ad- and abaxial arcs of stamens suggest one whorl ( Endress, 1986b ; Ren et al., 2007 ).

44 (new). Stamen positions (0) single, (1) double (at least in outer whorl). Double positions are recognized with reference to a previous or subsequent whorl; thus taxa with no perianth are scored as unknown. Single stamens scored as unknown (cf. character 43). See general references and those for characters 41 – 43. Nymphaeoideae uncertain because of high numbers refl ecting doubling in the perianth; Winteraceae: single relative to perianth in Takhtajania ( Endress et al., 2000 ) but double in Tasmannia ( Doust, 2000 ) and Pseudowintera ( Vink, 1970 ), Drimys irregular, thus (0/1); Canellaceae: presence in Cinnamosma and Capsicodendron ( Wilson, 1966 ) presumably derived; Tofi eldiaceae: double in Tofi eldia tenuifolia but not other species ( Leinfellner, 1962 ; Remizova and Sokoloff, 2003); Papaveraceae: double in Pteridophyllum , Fumaria , sometimes Hypecoum ( Murbeck, 1912 ); Ranunculaceae: double in Thalictrum presumably derived.

45 (DE 48). Stamen fusion (0) free, (1) connate. Taxa with one stamen rescored as unknown to avoid artifactual steps in reduction of a synandrous androecium to one. Ascarina : free based on pluristaminate species; Chloranthus : unknown because of uncertain interpretation of the androecium (see text; Endress, 1987b ; Doyle et al., 2003 ); Aristolochioideae changed from (1) to (0/1) because apparent fusion in Thottea may be due to fusion to the androgynophore ( Ding Hou, 1981 ; Leins et al., 1988 ; Endress, 1994c ).

46 (DE 70). Inner staminodes (0) absent, (1) present. Taxa with one stamen or one whorl of stamens rescored as unknown, since these conditions already preclude presence of inner staminodes. Hernandioideae changed from (0) to (1) based on recognition in Hernandia ( Endress and Lorence, 2004 ) and similar structures alternating with stamens in Illigera ( Kubitzki, 1969 ); Gyrocarpoideae from (0) to (0/1) based on presence in Hernandia but not Sparattanthelium ( Kubitzki, 1969 ).

47 (new). Glandular food bodies on stamens or staminodes (0) absent, (1) present. Calycanthoideae: present on stamens of Calycanthus and Sinocalycanthus but not in Chimonanthus ( Staedler et al., 2007 ).

Stamen characters (48 – 55): Endress and Hufford (1989) , Hufford and Endress (1989) , Endress (1994c) and references therein, plus the following for individual taxa: Aponogeton , Nartheciaceae, and Melanthiaceae: Endress (1996) ; Scheuchzeria : Cronquist (1981) ; Circaeaster : Junell (1931) , Hu et al. (1990) ; Hydrastis : Tamura (1995) .

48 (DE 49 modifi ed). Stamen base (0) short (2/3 or less the length of anther), (1) long ( > 2/3 length of anther) and wide ( > 1/2 width of anther), (2) long (2/3 or more length of anther) and narrow ( < 1/2 width of anther) (typical fi lament). Most scoring changes due to redefi nition of states. Barclaya : base less than half as long as the anther ( Tamura, 1982 ); Austrobaileya : base of the outer stamens almost as long as the anther; Lactoris : nearly sessile ( Bernardello et al., 1999 ); Aristolochioideae changed from unknown to (0/2) based on variation in Thottea ( Kelly, 1997 ); Eupomatia rescored (0/1) because of variation between species ( Hiepko, 1965 ; Endress, 1994c ); Atherospermataceae: all three types represented in Endress (1994c) , but (2) occurs only in Atherosperma , which is nested; Lauraceae: Hypodaphnis , most Beilschmiedia species, and Cryptocarya have a fi lament ( Fouilloy, 1965 ; Hyland, 1989 ); Berberidaceae: (0/2) because of short base in Nandina ( Hiepko, 1965 ; Terabayashi, 1983 ); Dioscoreaceae: (2) because Tacca (short) is too modifi ed to interpret; Platanus rescored as (0) with exclusion of fi lamentous fossils.

49 (DE 50). Paired basal stamen glands (0) absent, (1) present.


50 (DE 51 modifi ed). Connective apex (0) extended, (1) truncated or smoothly rounded, (2) peltate. See references for character 48. Nuphar : new peltate state; Chloranthaceae: Eklund et al. (2004) ; Magnoliaceae changed from (0) to (1) in Liriodendron , based on its relatively truncate apex, (0/1) in Magnolioideae based on variation within the group ( Endress, 1994c ); Proteaceae from (0/1) to (1): most basal groups are truncated except Placospermum , which is presumably derived ( Douglas and Tucker, 1996 ); Platanus rescored as (2) with exclusion of non-peltate fossils.

51 (DE 53). Pollen sacs (0) protruding, (1) embedded. Trimenia and Euptelea , at the limit between states in Doyle and Endress (2000) , have been changed from unknown to (0) because their sacs are perceptibly more protruding than those of otherwise comparable embedded taxa such as Ascarina and Trochodendraceae ( Endress and Sampson, 1983 ; Endress, 1987b ; Hufford and Endress, 1989 ).

52 (DE 52). Microsporangia (0) four, (1) two.

53 (DE 54 modifi ed). Orientation of dehiscence (0) distinctly introrse, (1) latrorse to slightly introrse, (2) extrorse. As discussed in Eklund et al. (2004) , including slightly introrse in (1) allows more taxa to be scored unambiguously, such as Ascarina , Hedyosmum , and Sarcandra , which would have varied internally under the old defi nition but can now be scored as (1). Changes in scoring of Cabombaceae, Nelumbo , Menispermaceae, Berberidaceae, and Proteaceae based on reexamination of references in Doyle and Endress (2000) with this new limit between states. This character is diffi cult to score in fl owers that consist of one stamen, because it is defi ned relative to the fl oral axis, which is generally not recognizable. The more readily visible orientation of the stamen relative to the infl orescence axis may or may not correspond to its orientation in the fl ower, depending on whether the stamen is located on the abaxial (anterior) or adaxial (posterior) side of the fl ower. In male fl owers of Hedyosmum and Ascarina (Chloranthaceae), the orientation of the stamen can be inferred from the position of the xylem in the vascular bundle (Endress, 1987b), which implies that the stamens are latrorse to slightly introrse (state 1). However, in Ceratophyllum , in which the stamens are extrorse relative to the multistaminate male structures, which we interpret as infl orescences, the vascular bundle is too reduced to determine the position of the xylem ( Endress, 1994b ), and we have therefore scored this genus as either introrse or extrorse (0/2). Latrorse stamens (as in Hydatellaceae) can be scored as such without information on stamen orientation.

54 (DE 55). Mode of dehiscence (0) longitudinal slit, (1) H-valvate, (2) valvate with upward-opening fl aps. Myristicaceae changed from (0/1) to (0) because H-valvate occurs only in Mauloutchia , now known to be nested ( Sauquet et al., 2003 ); Sarcandra and Chloranthus changed from (0) to (1) based on Endress (1987b , 1994c ) and Eklund et al. (2004) ; Liriodendron and Magnolioideae: Endress (1994c) ; Berberidaceae changed from (0/2) to (2) because the slit dehiscence of Nandina can now be interpreted as derived. In Calycanthoideae, Sinocalycanthus is H-valvate ( Staedler et al., 2007 ), but this is presumably derived. Ranunculaceae: Tobe and Keating (1985) .

55 (DE 56). Connective hypodermis (0) unspecialized, (1) endothecial or sclerenchymatous. Dioscoreaceae: our observations on Dioscorea .

Characters 56 – 58: Yakovlev (1981 , 1990 ); Amborella : Tobe et al. (2000) ; Siparunaceae: Kimoto and Tobe (2003) ; Gomortega : Heo et al. (2004) ; Hernandioideae: Heo and Tobe (1995) .

56 (DE 57). Tapetum (0) secretory, (1) amoeboid. Furness and Rudall (2001) ; Nuphar changed from (1) to (0): Furness and Rudall (2001) ; Aristolochioideae from (0) to (?): Furness and Rudall (2001) list Asarum as the only member of Aristolochiaceae studied; Atherospermataceae: Furness and Rudall (2001) ; Hydrastis : Tobe and Keating (1985) ; Ceratophyllum : Shamrov (1983b) .

57 (DE 58). Microsporogenesis (0) simultaneous, (1) successive. Nuphar : Batygina and Shamrov (1983) ; Aponogeton , Nartheciaceae: Furness and Rudall (1999) ; Scheuchzeria : Yakovlev (1990) ; Melanthiaceae: Eunus (1951) ; Ceratophyllum : Les (1993) .

58 (new). Pollen nuclei (0) binucleate, (1) trinucleate. Brewbaker (1967) ; Austrobaileya , Eupomatia , Calycanthoideae, Atherospermataceae, Monimiaceae, Melanthiaceae: Yakovlev (1981) ; Cabomba , Brasenia , Nuphar , Barclaya , Nelumbo : Batygina and Shamrov (1983) , Gabarayeva et al. (2003) , Nuphar and Nymphaeoideae scored (0/1) because of confl icts with Brewbaker (1967) and Yakovlev (1981) ; Trimenia : Endress and

Sampson (1983) ; Lactoris : Kamelina (1997) ; Galbulimima : Prakash et al. (1984) ; Hortonia : Kimoto and Tobe (2001) ; Tofi eldiaceae: Wunderlich (1936) ; Butomus : Cronquist (1981) ; Aponogeton : van Bruggen (1998) ; Circaeaster : Junell, 1931; Hydrastis : Tobe and Keating (1985) .

Pollen characters 59 – 73: see Doyle (2005) for updated interpretation and references on taxa treated therein. Walker (1976a , b ) and Sampson (2000a) consulted throughout. Sources of data for taxa added or split since Doyle (2005) : Hydatellaceae: Linder and Ferguson (1985) ; Liriodendron and Magnolioideae: reviewed in Doyle (2005) ; Aponogeton : Thanikaimoni (1985) ; Scheuchzeria : Zavada (1983) , Grayum (1992) ; Nartheciaceae: Takahashi and Kawano (1989) , Caddick et al. (1998) ; Dioscoreaceae: Schols et al. (2005) ; Melanthiaceae: Halbritter and Hesse (1993) ; Circaeaster : Nowicke and Skvarla (1982) ; Glaucidium and Hydrastis : Nowicke and Skvarla (1979 , 1981 ); Ceratophyllum : Takahashi (1995) , scored as unknown for structure characters because of extreme exine reduction.

59 (DE 59). Pollen unit (0) monads, (1) tetrads.

60 (DE 62). Pollen size (average) (0) large ( > 50 µ m), (1) medium (20 – -50 µ m), (2) small ( < 20 µ m), ordered. Acorus changed from (1) to (2) based on Erdtman (1952) and Grayum (1992) .

61 (DE 60 modifi ed). Pollen shape (0) boat-shaped, (1) globose, (2) triangular, angulaperturate (Proteaceae).

62 (DE 61 modifi ed). Aperture type (0) polar (including sulcate, ulcerate, and disulcate), (1) inaperturate, (2) sulculate, (3) (syn)tricolpate with colpi arranged according to Garside ’ s law, with or without alternating colpi, (4) tricolpate.

63 (new). Distal aperture shape (0) elongate, (1) round. Taxa with several or no apertures scored as unknown.

64 (new). Distal aperture branching (0) unbranched, (1) with several branches. Taxa with several or no apertures scored as unknown.

65 (DE 63). Infratectum (0) granular (including “ atectate ” ), (1) intermediate, (2) columellar, ordered.

66 (DE 64). Tectum (0) continuous or microperforate, (1) perforate (foveolate) to semitectate (reticulate), (2) reduced (not distinguishable from underlying granules). Glaucidium , Hydrastis , core Ranunculaceae: Nowicke and Skvarla (1979 , 1981 ).

67 (new). Grading of reticulum (0) uniform, (1) fi ner at ends of sulcus (liliaceous), (2) fi ner at poles (rouseoid). Scored only in taxa with state (1) in character 66. References cited in Doyle (2005) for taxa covered therein. Both uniform ( Nandina ) and rouseoid ( Leontice , Caulophyllum ) occur in near-basal Berberidaceae ( Nowicke and Skvarla, 1981 ). Scheuchzeria scored as unknown because it is inaperturate.

68 (DE 65). Striate muri (0) absent, (1) present. Glaucidium , Hydrastis , core Ranunculaceae: Nowicke and Skvarla (1979 , 1981 ). Buxaceae changed from (1) to (0/1) because both states occur in Buxus ( K ö hler, 1981 ; K ö hler and Br ü ckner, 1982 ).

69 (DE 66). Supratectal spinules (smaller than the width of tectal muri in foveolate-reticulate taxa) (0) absent, (1) present. Cabomba (0/1) based on spinules in C. palaeformis ( Ø rgaard, 1991 ); Glaucidium spinules ( Nowicke and Skvarla, 1981 ); Hydrastis smooth ( Nowicke and Skvarla, 1982 ).

70 (DE 67). Prominent spines (larger than spinules, easily visible with light microscopy) (0) absent, (1) present.

71 (DE 68). Aperture membrane (0) smooth, (1) sculptured. Winteraceae changed from (?) to (1) based on the sculptured ring around the ulcus. Winteraceae changed from (?) to (1) because they have fi ne verrucae either on the ring of thickened exine around the pore or across the pore ( Praglowski, 1979 ; Sampson, 2000b ); Hydrastis strongly sculptured ( Nowicke and Skvarla, 1982 ), Glaucidium not expanded enough in Nowicke and Skvarla (1981) to score.

72 (DE 69 modifi ed). Extra-apertural nexine stratifi cation (0) foot layer, not consistently foliated, no distinctly staining endexine or only problematic traces, (1) foot layer and distinctly staining endexine, or endexine only, (2) all or in part foliated, not distinctly staining ( Doyle, 2005 ).

73 (new). Nexine thickness (0) absent or discontinuous traces, (1) thin (less than 1/3 of exine) but continuous, (2) thick (1/3 or more of exine), ordered ( Doyle, 2005 ).


Old and new gynoecial characters (74 – 96): Endress and Igersheim (1997, 1999 , 2000a , b ), Igersheim and Endress (1997 , 1998 ), Igersheim et al. (2001) , and references therein, plus the following for individual taxa: Amborella : Endress and Igersheim (2000b) , Buzgo et al. (2004) ; Brasenia : Endress (2005) ; Winteraceae: Endress et al. (2000) ; Hydatellaceae: Rudall et al. (2007) ; Aponogeton , Scheuchzeria : Igersheim et al. (2001); Melanthiaceae: El-Hamidi (1952); Nartheciaceae: Remizowa et al. (2006) ; Circaeaster , Hydrastis : Endress and Igersheim (1999) ; Glaucidium : Tamura (1972) , Tobe (2003); Ceratophyllum : Endress (1994b) , Igersheim and Endress (1998) .

74 (DE 71). Carpel number (0) more than one, (1) one.

75 (DE 72). Carpel form (0) ascidiate up to stigma, (1) intermediate (both plicate and ascidiate zones present below the stigma) with ovule(s) on the ascidiate zone, (2) completely plicate, or intermediate with some or all ovule(s) on the plicate zone.

76 (DE 73 part). Postgenital sealing of carpel (0) none, (1) partial, (2) complete. Saarela et al. (2007) scored Hydatellaceae as unknown, but Rudall et al. (2007) confi rmed the lack of postgenital fusion.

77 (DE 73 part). Secretion in area of carpel sealing (0) present, (1) absent. Rudall et al. (2007) reported no mucilage in Hydatellaceae, but because of the diffi culty in detecting mucilage and its potential artifactual loss in such material, we score them as unknown. Trochodendron and Tetracentron : Endress and Igersheim (1999) .

78 (DE 74). Pollen tube transmitting tissue (0) not prominently differentiated, (1) one layer prominently differentiated, (2) more than one layer prominently differentiated.

79 (DE 75). Style (0) absent (stigma sessile or capitate), (1) present (elongated apical portion of carpel distinctly constricted relative to the ovary). Hedyosmum changed from (0/1) to (1), Asaroideae from (1) to (0/1) following Eklund et al. (2004) . In Ceratophyllum Endress (1994b) and Iwamoto et al. (2003) showed that the apical extension, on the side where the ovule is attached, is ventral and therefore not comparable to a style. However, the opening of the canal just below this is almost halfway up a long, narrow extension of the carpel above the ovary, which we score as a style (cf. Shamrov, 1983a ).

80 (DE 76). Stigma (0) extended (half or more of the style – stigma zone), (1) restricted (above slit or around its upper part). Hydatellaceae scored as unknown because the stigma is reduced to a few long, uniseriate papillae. Ceratophyllum scored as unknown because it lacks differentiated stigmatic tissue ( Endress, 1994b ; Iwamoto et al., 2003 ).

81 (DE 77 part). Multicellular stigmatic protuberances or undulations (0) absent, (1) present. See text for discussion of this and character 82. Berberidaceae: Hydrastis -like protuberances in Nandina , Podophyllum , and Jeffersonia but not other genera ( Endress and Igersheim, 1999 ) are presumably derived. Hedyosmum and Ascarina have both protuberances and unicellular papillae ( Endress, 1987b ).

82 (DE 77 part, modifi ed). Stigma papillae (most elaborate type) (0) absent, (1) unicellular or with a single emergent cell and one or more small basal cells, (2) uniseriate pluricellular with emergent portion consisting of two or more cells. State (0) split from unicellular or absent, since lack of papillae is potentially informative with splitting of Sarcandra and Chloranthus and addition of Ceratophyllum ; (1) redefi ned to include papillae with small, sunken basal cells, which transfers Cabombaceae from pluricellular to unicellular, and Nymphaeoideae from uni/pluricellular to pluricellular.

83 (DE 78). Extragynoecial compitum (0) absent, (1) present. Annonaceae changed from (0/1) to (1) following Sauquet et al. (2003) ; Buxaceae from (?) to (0/1) based on von Balthazar and Endress (2002b); Tofi eldia from (0) to (?) based on Igersheim et al. (2001) . Confi rmed in Schisandraceae ( Lyew et al., 2007 ) and all four genera of Calycanthaceae, including Idiospermum (Staedler et al., 2009).

84 (DE 79). Carpel fusion (0) apocarpous (including pseudosyncarpous), (1) parasyncarpous, (2) eusyncarpous (at least basally). Taxa with one carpel rescored as unknown to avoid artifactual steps in reduction of a syncarpous gynoecium to one carpel. Winteraceae rescored (0/1) because of parasyncarpy in Takhtajania ( Endress et al., 2000 ).

85 (DE 80). Oil cells in carpels (0) absent or internal, (1) intrusive. Taxa with no oil cells in any tissue rescored as unknown. Myristicaceae changed from (0) to (0/1) based on Sauquet et al. (2003) .

Characters 86 – 88: general gynoecium references cited above and unpublished data of Endress and Igersheim.

86 (new). Long unicellular hairs on and/or between carpels (0) absent, (1) present.

87 (new). Short, curved, appressed, unlignifi ed hairs with up to two short basal cells and one long apical cell on carpels (0) absent, (1) present ( Endress, 2001 ). Endress (2001 , 2005 ); Hydatellaceae: Rudall et al. (2007) .

88 (new). Nectary on dorsal or lateral sides of carpel or pistillode (0) absent, (1) present. Not found in all Buxaceae, but apparently ancestral (von Balthazar and Endress, 2002b).

89 (DE 81). Septal nectaries or potentially homologous basal intercarpellary nectaries (0) absent, (1) present. Nartheciaceae: absent in Lophiola ( Tamura, 1998 ) and our material of Narthecium , but Utech (1978) reported septal pockets between the carpels in Aletris (including Metanarthecium ), so scored (0/1).

90 (DE 82 modifi ed). Number of ovules per carpel (0) one, (1) two or varying between one and two, (2) more than two. This recognizes production of strictly one ovule as most distinctive. Schisandraceae: analyses that nest Kadsura in Schisandra ( Liu et al., 2006 ) strengthen the assumption that two ovules are ancestral; Saururaceae: changed from (1/2) to (2) because the biovulate genus Saururus appears to be nested ( Meng et al., 2002 , 2003 ); Magnoliaceae were formerly (1), the most parsimonious scoring if Liriodendron is (1), Magnolioideae (1/2), but now the two are separated; Araceae changed from (0) to (0/1) because of variation and uncertain relationships among basal groups; Euptelea changed from (0/1) to (1) because variation between one and rarely two in E. polyandra now falls in state (1).

91 (DE 83 modifi ed). Placentation (0) ventral, (1) laminar-diffuse or “ dorsal. ” “ Dorsal ” ovules, commonly seen in Brasenia ( Endress, 2005 ), are attached to the inside of the carpel on its midrib. Ceratophyllum appears “ dorsal, ” but development shows it is ventral ( Igersheim and Endress, 1998 ; Iwamoto et al., 2003 ). Rudall et al. (2007) reaffi rm that position in Hydatellaceae is uncertain.

92 (DE 84). Ovule direction (0) pendent, (1) horizontal, (2) ascendent. Barclaya changed from (1) to (?) based on irregular orientation described by Igersheim and Endress (1998) . Barclaya changed from (1) to (?) because of excessive variation ( Igersheim and Endress, 1998 ); Dioscoreaceae changed from (0) to (0/1) because Stenomeris appears to be horizontal ( Dahlgren et al., 1985 ); Hydrastis has one pendent and one ascendent ovule ( Endress and Igersheim, 1999 ), scored as (0/2).

93 (DE 85). Ovule curvature (0) anatropous (or nearly so), (1) orthotropous (including hemitropous).

94 (DE 86). Integuments (0) two, (1) one.

95 (DE 91). Chalaza (0) unextended, (1) pachychalazal, (2) perichalazal. Because pachychalazal strictly applies only to anatropous ovules (cf. Periasamy, 1962 ), we have rescored orthotropous taxa as unknown.

96 (DE 92 modifi ed). Nucellus (0) crassinucellar (including weakly so), (1) tenuinucellar or pseudocrassinucellar. Tenuinucellar is defi ned in terms used for rosids ( Endress and Matthews, 2006 ), with conditions in basal groups corresponding to incompletely tenuinucellar; completely tenuinucellar exists mostly in asterids. Gomortega : Heo et al. (2004) .

Fruit and seed anatomy characters (97 – 104) based primarily on Corner (1976) and Takhtajan (1985 , 1988 , 1991 ); Hydatellaceae: Hamann (1975) , Hamann et al. (1979) ; Atherospermataceae, Gomortega : Doweld (2001) ; Tofi eldiaceae: Oganezova (1984) ; Proteaceae: rescored based on Bellendena and Persoonioideae as described by Venkata Rao (1960 , 1961 , 1971 ).

97 (DE 93 part). Fruit wall (0) wholly or partly fl eshy, (1) dry. State (1) includes green but not juicy, as in Cabombaceae. Drupes, previously treated as a third state, are specifi ed by the next character. Hedyosmum changed from fl eshy/endocarp to dry because the fl eshy tissue is at the surface of the inferior ovary and may therefore not be gynoecial ( Endress, 1987b ); Saururaceae from fl eshy/dry to fl eshy following


Takhtajan (1988) ; Dioscoreaceae from fl eshy/dry to dry because berries occur in most but not all members of Tacca , and other taxa are dry ( Kubitzki, 1998 ).

98 (DE 93 part). Lignifi ed endocarp (0) absent, (1) present. Taxa with dry fruit wall scored as unknown. Piperaceae changed from fl eshy/endocarp to (0) because descriptions of “ drupes ” do not describe an actual lignifi ed endocarp ( Takhtajan, 1988 ; Prakash and Kin, 1982 ); Proteaceae scored as (1) based on fl eshy persoonioids.

99 (DE 94 modifi ed). Fruit dehiscence (0) indehiscent or dehiscing irregularly, dorsally only, or laterally, (1) dehiscent ventrally or both ventrally and dorsally, (2) horizontally dehiscent with vertical extensions. Defi nitions of states (0) and (1) inadvertently reversed in Doyle and Endress (2000) ; (2) added for Papaveraceae and some Berberidaceae. Hydatellaceae: some species dehisce along the vascular bundles of the single carpel ( Rudall et al., 2007 ), but whether this is ancestral or derived within Hydatellaceae, it is not comparable with dehiscence in other taxa, so we score the family as (0). Saururaceae changed from (0/1) to (0) because Saururus , the only indehiscent genus ( Takhtajan, 1988 ), now appears to be nested; Aristolochioideae from (1) to (?) because they are septicidal rather than ventrally dehiscent ( Huber, 1993 ); Berberidaceae from indehiscent to (0/2) because Caulophyllum , Gymnospermium , Leontice , and many Epimediineae have horizontal dehiscence ( Loconte, 1993 ); Platanus changed from (0/1) to (0) with elimination of dehiscent fossils.

100 (DE 95). Testa (0) slightly or nonmultiplicative, (1) multiplicative. Myristicaceae changed from (1) to (0) based on Sauquet et al. (2003) .

101 (DE 96). Exotesta (0) unspecialized, (1) palisade or shorter sclerotic cells, (2) tabular, (3) longitudinally elongated, more or less lignifi ed cells. State (3) added for Aponogeton and Scheuchzeria ( Takhtajan, 1985 ). Tofi eldiaceae changed from (2) to (0/2); Proteaceae from (0/1) to (0).

102 (DE 100). Ruminations (0) absent, (1) testal, (2) tegminal and/or chalazal. Following Sauquet et al. (2003) , state (1) is restricted to testal ruminations,

Myristicaceae are changed from (0) to (2), and Galbulimima is changed from from (0) to (?) because of probable but reduced ruminations ( Doweld and Shevyryova, 1998 ). Hernandioideae changed from (?) to (1/2) because the ruminations have been variously described as from the chalaza ( Corner, 1976 ) and the mesotesta ( Takhtajan, 1988 ).

103 (DE 101). Operculum (0) absent, (1) present.

104 (DE 102). Aril (0) absent, (1) present. Myristicaceae changed from (0/1) to (1): an aril is reconstructed as ancestral by Sauquet et al. (2003) .

105 (new). Female gametophyte (0) four-nucleate, (1) eight- or nine-nucleate. Tetrasporic types in Piperaceae scored as unknown. Williams and Friedman (2004); Amborella : Friedman (2006) ; Hydatellaceae: Hamann (1975) ; Melanthiaceae: Yakovlev (1990) ; Nartheciaceae: Zomlefer (1997b) ; Dioscoreaceae: Huber (1998) ; Circaeaster : Junell (1931) , Hu and Yang (1987) .

106 – 110: Yakovlev (1981 , 1990 ), Takhtajan (1985 , 1988 , 1991 ); Amborella : Tobe et al. (2000) ; Hydatellaceae: Hamann (1975) ; added monocots: Kubitzki (1998) , Zomlefer (1997a – c ); Ranunculaceae: Tobe and Keating (1985) .

106 (DE 103). Endosperm development (0) cellular, (1) nuclear, (2) helobial. Amborella , Nuphar , Illicium : Floyd and Friedman (2001) ; Gomortega : Heo et al. (2004) ; Siparunaceae: Kimoto and Tobe (2003) ; Hernandioideae: changed from (1) to (0) based on Heo and Tobe (1995) ; Circaeaster : Junell (1931) , Hu and Yang (1987) .

107 (DE 104). Endosperm in mature seed (0) present, (1) absent. Nikiticheva and Proskurina (1992) described Scheuchzeria as having endosperm present as a thin fi lm around the embryo, but this is not clearly different from similar tissue in Butomus ( Takhtajan, 1985 ), so we score Scheuchzeria as (?).

108 (DE 105 modifi ed). Perisperm (0) absent, (1) from nucellar ground tissue, (2) from nucellar epidermis. State (2) added for Acorus ( Rudall and Furness, 1997 ).

109 (DE 106). Embryo (0) minute (less than 1/2 length of seed interior), (1) large.

110 (DE 107). Cotyledons (0) two, (1) one.


1 2 3 4 5 6 7 8 9 0 1

12345678901234567890123456789012345678901234567890123456789012345678901234567890123456789012345678901234567890

Amborella 1?000000010000010000010001100000?20001000?20000100000000100110?020?01011100000001210?010000010?001000000100000Cabomba 11010110A1000?011111020000000001012?110010010?02010020001000000020?1A010100000100100?010021000001?001010020100Brasenia 1101?11001?0000110100?00?0000001012?000010210002010010000100000020?0001010000?100100?010011000??1?001010?20100Nuphar 1101011000100?0110001200000000010211000012210000021001000A00000010?01111100200000112?0000210000000001011000100Barclaya 1101011000?00?0110001200?020000122100000122?00000010000??00112??20?000???012000002?2?010021?10?00000?010000100Nymphaeoideae 1101011000101001100012002020010122100000122?0001001000000A0012??10?000?1200200000212?010021000A000001011000100Hydatellaceae 1101210000000002???0021021?00?1???????01??????0201?0100??002000020?010?01100??0?02???01000?000001?00101000010?Austrobaileya 10000000100000010000000000000000?21000000?20010100000000000110002100001110000110011000000201002000010100??0000Trimenia A000000010000?0A0000010A0A000?00?20000000?D000020000D000000112??210010111100000012??A0A000000000000010000?0000Illicium 00000000000000000000100000000100?21000000?D0000101000000000113??210000111011011001101000000200001?1A1000000000Schisandraceae 1000000000000?0000001B0001010000?21000000?E010010100B000000113??2100001110000100011010000101000000001000000000Hedyosmum A000?00010?12?000000021111200?0100A??001??????000E10101?00011001210010102100001011??0000000010?01?000000100000Ascarina 1000000010012?000000020101?00?1???????0A??000?000010101???011000210010102100000011??0000000010?000000000??0000Sarcandra 1000000010012?000000?20100?00?1???????01??????010110110000011???210000102100000000??1000000010?000010000100000Chloranthus 10000000100120000000020100?00?1???????0???????0A0000010000011???21000011D100000010??1000000010?000000000100000Liriodendron 0010A000000130000000000000012001021000100?200000011020?00000000020?000021022001101000000010100001?010000100000Magnolioideae 0010A0000A013000000010000001200102D000100?2000000A100A0000000000D0?0000210220010010000000D0100001?110000100000Degeneria 00101000011000000000000000001000?21001000?200110001021000000000000?0000?0122110002??00000201000000110100100000Galbulimima 001000000110000000000000000110????????100?200110001021001001100000?0000?002?010101100??00001000001000?001?0000Eupomatia 0000100001100000000000000010001???????100?20111A00100100000112??00?0000210?21101021?000002010000000101001?0000Annonaceae 0010100001100000000011000000A0010210000010210AA000102110A000000000?00002102101A101100A000D0D0020A0A10100100000Myristicaceae 00100000010000000000120AB1000?0100A??100A00?1?0?010020001001100021000012D112000101??AA000002001000100201110000Calycanthoideae 000010001000000A0000000000100000?21000000?2001A0000020000A0112??2100000210221011011?0100010200001?010000101010Idiospermum 00?0100010000?000000?00000100000?2100?000?2001000000200???0112???0?000???A2210011??001000102000?1?00?000??1010Atherospermatac 00001000100000000000010000100000?21000000?20010A1A11E20000011000210000A21011001101100100000200001?0000001?0000Siparunaceae 000010001000000000000210?110?00??AA???00????0?0A01110200100211??10?010?210110011011000000002010001000000100000Hortonia 0000100010?00?011000010000100000?21000000?D001021100200??00111???0?010??001101110110110000000000010000001?0000Monimioideae 0000A00010000000000001000110?00??DA00000??2?0?0211000100100111??10?001??001100110110110000000000010000001000?0Mollinedioideae 0000100010?00?000000010001100001DD000?001DDA0?000100000010AD11??1B?0AA??0000000001100A0000000000010000001?00A0Gomortega 0000100010?00000000001000020?000?20000000??0010211110200000111??10?010??0012101101??0000000010?001000000?00010

Lauraceae 00001000A000000AA000010000200?010100000010200102111A020A100111??02?001??1112121101??0A00000000100A010000111010Hernandioideae 000010000000000110A0021000200?01EDB000001210010211110201100011??02?001??1112121101??0100000000A001010D00101010Gyrocarpoideae 00?0100000?00001100A021000200?01200??A0012A00A0211112201100111?????0?1???112121101??01000000000001010000101010Winteraceae 0000A00000000000000001000000000112100100122A000101002010001110102100001110221100010A00000201000000001000100000Canellaceae 0000100000000?0000000A00000000010D1001001210100?0100200000011000210000002021010?01?100000D0100000000100A1?0000Saururaceae 1000000001111001100002010020001???????00101?0002011010000002100020?000102022101001011000020110?000100000100100Piperaceae 100000000A111?01100002010000001???????001AA?00020110A0000002100020?0101010?210A?01?1100000?210?000000000?A0100Lactoris 1000000001111?00100001000A00000100A??00010100000000020000111101010?000001022101001000000020100011?100000100000Asaroideae 100020000110000110000000002000010AAA010010D100020000200000011A002A000011102211A002020000020100001?100000100000Aristolochioideae 1000100001100001100002100020000100A??10010A1A00B010020??A00111??20?0A0?11022100?01?20000020100001??1A000100000

Euptelea 000000000000000AA00002000000001???????001?0?0?0200001110000114??21001011101210000100?000010000001?002000100000

Papaveraceae 1000001000?A0?0110010D000000000112A1000011A100020100200A000114??2A?0A011D020001?01?1?000020000001?201000110000

Lardizabalaceae A0000000000000011001020001000001022110001010A00201002000000114??20?00011102101010110?0000B01000000011000100000

Circaeaster 1000??0000?00?0?1100010000000000?0A??0000?000?0201010000000114??20?1001??A00000101?0?000010011011?000000100000

Menispermaceae A000000A000000011000010A0100000102A110001010A0020100A000000214??21000011102100A1AA10?A000102000001000A00110010

Berberidaceae 1000000000?1A?01100101000000A?010211A0001010000B0100E20A000114??21B00011D10001A000???000020D000000BA100A110000

Glaucidium 10??0?0001??0?011001?0000000200111200000??2?00020100?0????0114??210010?1202???011?00???0020100?11?101000?10010

Hydrastis 10000?0001?10?01100100000000000100A??000??2?0001010010?0?00114??2101001120221?111000?100020B00001?101000?10000

Core Ranunculac 1000000000?10?011001010000000000?12110000?20000201001000000114??20?01011102211110100?A000E0?00011?101000110000

Nelumbo 10010?1001111?011010000000000000?2100000??2000020000D000010014??21000011100001000100?000000000101?000000111010

Platanus 0000000001111?0010010D0121000001B10000001EA0000002A01110000114??21000011202211100100???0010010?01?000000110010

Proteaceae 0000000000000000100AA20000000?01110000001110000201000000000124??2A0000?02122111101???000010010?0A10A000011A010

Tetracentron 00000000010110011000?D0100200001110000001110000201101110000114??212100112022111001?2?001020000001?1020001?0000

Trochodendron 000000000000000?A0001100002010????????00A220000201101110000114??21210011202201100102?001020000001?102000100000

Buxaceae 0000?000A000000A1000010A01000001110000001110000200000010000114??210A001?102211100102?00101000000A0A010001000A0Acorus 100120000111011220000201200000010100000010100002010000001002000020?000011012010101?2A00002?010?100000000100201Tofi eldiaceae 1001200001?10012200002A00000000101000000101A0002010000?00001000021100000102201110100?000120100001?10A000120011

Butomus 110120000111010220000210000000010110000010110002010020011101000021100000102101110200?000121200001?102000121011

Aponogeton 11012110???1010120000201200000010AB0000010100002010020?1A101A00001001010102101110100?000020200001??03000121011

Scheuchzeria 1101200001?10112200001000000?0010100000010100002000020?111?111??21?000???02101110100?000010D00001?10300012?011

Araceae 10012AA101110A0DD000020120000001A10000001A100001010020?1100100002A?000011AA0010A0E?2?0000A0BAA0000000000120011

Nartheciaceae 100120000A?100A2200002000000?0010120000010100002010000?01?01000021100000102101110102?000A20200001?101000120001

Dioscoreaceae 1001200100?AA00110000D00002000010120000010100002010000000001000020?0000010210111010D?0001D0A00001?A000001100A1

Melanthiaceae 1001200100?1000220000200000000010120?00010100002010020?01001000021100010102101110102?000020200001?101000120001

Ceratophyllum 110101001000000??1010201D1?00?1???????01??????000?10B000A00111???????????100001?00???000000011?01?000000100010

Archaefructus inf 1???????0??00?011101?20021?0?01????????0??0?0??000????????010000?0?000???A????1????0?????200????1???1?????????

Archaefructus fl o 1???????0??00?011101?0000001??1????????0??2?0??00?????????010000?0?000???0????1????0?????200????1???1?????????

Archaefructus NF 1???????0??00?011101?20021?0?01????????0??0?0??000???????????????????????A????1????0?????200????1???1?????????

Table 2. Complete data matrix, including infl orescence and fl oral characters and other characters relevant for placement of Ceratophyllum and Archaefructus . A = 0/1, B = 0/2, C = 0/4, D = 1/2, E = 0/1/2.


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Reconstructing the ancestral angiosperm flower and its initial specializations

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