The Relationships of Vascular PlantsAuthor(s): P. KenrickReviewed work(s):Source: Philosophical Transactions: Biological Sciences, Vol. 355, No. 1398, BryophytePhylogeny and Interrelationships with Early Embryophytes (Jun. 29, 2000), pp. 847-855Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/3066809 .Accessed: 17/02/2012 02:10Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jspJSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact firstname.lastname@example.org. The Royal Society is collaborating with JSTOR to digitize, preserve and extend access to Philosophical Transactions: Biological Sciences.http://www.jstor.org
B4 - THE ROYAL9;@ SOCIETY The relationships of vascular plants P. Kenrick Department Palaeontology, JWatural of The HistoryMuseum, Cromwell Road,London SW7 5BD, UK (p.kenrick@,nAm.ac.uk) Recent phylogenetic research indicates that vascular plants evolved from bryophyte-like ancestors and that this involved extensive modifications to the life cycle. These conclusions are supported by a range of systematic data, including gene sequences, as well as evidence from comparative morphology and the fossil record. Within vascular plants, there is compelling evidence for two major clades, which have been termed lycophytes (clubmosses) and euphyllophytes (seed plants, ferns, horsetails).The implications of recent phylogenetic work are discussed with referenceto life cycle evolution and the interpretationof stra- tigraphic inconsistencies in the early fossil record of land plants. Life cycles are shown to have passed through an isomorphic phase in the early stages of vascular plant evolution. Thus, the gametophyte generation of all living vascular plants is the product of massive morphological reduction. Phylogenetic researchcorroboratesearlier suggestionsof a major representationalbias in the early fossil record. Mega- fossils document a sequence of appearance of groups that is at odds with that predicted by cladogram topology. It is argued here that the pattern of appearance and diversificationof plant megafossils owes more to changing geological conditions than to rapid biological diversification. Keywords: vascular plant; bryophyte; phylogeny; life cycle Remarkable developments in phylogenetics over the past 1. INTRODUCTION 20 years are beginning to resolve some of these seeminglyThe development of a robust phylogenetic frameworkfor insoluble problems and have brought the remainingvascular plants is widely perceived as crucial to address- critical questions into much sharper focus. It is clear nowing a raft of important issues concerning the origins of that all land plants share a common terrestrialorigin andthe terrestrial flora, life cycle evolution and morpho- that vascular plants probably are in an importantgenesis in plants. Recent work has shown that the relation- evolutionary sense just bryophyteswith a highly modi-ships of vascular plants must be evaluated within the fied life history.broader context of land plants as a whole. Yet, deep phylo- This new perspective on the evolution of vasculargenetic questions such as these are difficult to resolve, not plants and bryophytes has emerged from several decadesleast because the early evolution of the land flora took of phylogenetic research. Key developments include theplace over 400 Myr ago (Late Silurian-Early Devonian). application of transmission electron microscopy (TEM)Numerous phylogenetic hypotheses have been proposed, to the study of cell ultrastructure and cell division ingiving rise to a bewildering diversity of ideas, some of green algae and land plants (Mattox & Stewart 1984;which are reflected in current taxonomic practice Pickett-Heaps& Marchant 1972;Stewart & Mattox 1975).(Kenrick & Crane 1997a). One of the legacies of this These data cut across insuperable difficulties at thechequered systematic history is the broad acceptance of a cellular level to give a truly comparable subcellular dataclassification that groups land plants into two categories, set from green algae to gymnosperms. The application oftermed vascular plants (tracheophytes)and bryophytes. cladistic methods has also had a major impact throughAll land plants can be classified into one of these groups the development of a rational and explicit way ofon the basis of their life cycles and the extent to which choosing among competing phylogenies. Using a cladisticthe diploid spore-bearing (sporophyte) and haploid approach, Mishler & Churchill (1984, 1985) showed thatgamete-bearing (gametophyte) phases develop. Bryo- the diverse data of comparative morphology are mostphytes possess a small, parasitic sporophyte, which is simply explained by a hypothesis of land plant mono-little more than a simple sporangium, borne on a larger, phyly. Controversially,this analysis indicated that mossesthalloid or leafy gametophyte. The life cycle of vascular are more closely related to vascular plants than they areplants is the antithesis of that in bryophytes. Here the to liverworts. In other words, bryophytes are a para-sporophyte is independent, morphologically complex and phyletic group. More recently, molecular data on genefrequently a very large organism. These striking differ- sequencesand genome structurehave provided a wealth ofences in life history create additional problems for phylo- new information from chloroplast, mitochondrion andgenetics by obscuring the crucial morphological nucleus (Crowe et al. 1997; DuS & Nickrent 1999;comparisons necessary for constructing a robust phyloge- Hedderson et al. 1998; Kranz et al. 1995; Lewis et al. 1997;netic tree. This difficulty is further exacerbated by the Malek et al. 1996; Mishler et al. 1994; Nishiyama & Katoeven larger disjunction between land plants and their 1999;Qiu et al. 1998). Results corroboratethe paraphylyofclosest relatives in the green algae (Charophyceae). bryophytes, but they are less clear about the relationshipsPhil. Trans. SOG. R. Lond.B (2000) 355, 847-855 847 C)2000 The Royal Society
848 P. Kenrick Relationshitsofrascularplants (a) tracheophytes MP tree (vascularplants) euphyllophytes lycophytes Rhyniopsidat Aglaophytont i protracheophytes Horneophytont - mosses hornworts | bryophytes liverworts (b) tracheophytes trees + 2 steps (vascularplants) euphyllophytes lycophytes Rhyniopsidat Aglaophytont protracheophytes Horneophytont mosses hornworts bryophytes liverworts (c) tracheophytes trees + 3 steps euphyllophytes lycophytes Rhyniopsidat mosses bryophytes hornworts liverworts l protracheophytes Aglaophytont HorneophytontFigure1. Summary cladograms relationships of amongbasalland plantsfromthe phylogenetic studyof living and fossilspeciesby Kenrick& Crane(1997a). t=extinct taxon. (a) Mostparsimonious (MP) treeshowingbryophytes paraphyletic vascular toplants.Earlymegafossils into the vasularplant stemgroup.(b) Treestwo stepslongerthan the mostparsimonious fall treeresolvedbryophytes a monophyletic sistergroupto vascularplants.(c) Treesthreestepslongerthan the mostparsimo- as andnioustreeresolvedprotracheophytes paraphyletic bryophytes vascularplants. as to andof various bryophyte groups to vascular plants. This hornworts, mosses).The first detailed cladistic analysis ofpaper reviews recent phylogenetic developments and this problemwas based on the comparativemorphology ofexamines some of their consequences for life cycle evolu- living species (Mishler & Churchill 1984, 1985). Resultstion and the interpretationof stratigraphicpatterns in the indicated that whereasthese four groups are monophyletic,early fossil record of land plants. some bryophytes (i.e. mosses) are more closely related to vascular plants than they are to other bryophytes (Mishler & Churchill 1984, 1985; figure 1). Specifically, 2. PHYLOGENETIC OVERVIEW this controversialresult implied that mosses and vascular (a) Vascular plants and bryophytes plants share a common ancestor with a bryophyte-like life One of the key phylogenetic questions in plant history and that there has been a major shift in life cyclesystematics is the nature of the relationship between from gametophyte-dominated to sporophyte-dominatedvascular plants and the other major living groups of land in the lineage leading to vascular plants. Subsequentplants, collectively termed bryophytes (i.e. liverworts, phylogenetic studies based on comparative morphology,Phil. Trans. SOG. R. Lond.B (2000)
Relationshipsofrassularplants P. Kenrick 849gene sequences and genomic structure continue to favour closest relatives in the green algae (Charophyceae).Thereparaphyly of bryophytes, but there is as yet no consensus are enormous diffierencesbetween the gametophytes ofon the precise nature of the relationships among these land plants and those of the charophycean algae. Also,four major plant groups. sporophytes are absent from charophycean algae, and A moss + vascular plant clade is supported by several there is no compelling fossil evidence for stem group landmorphological analyses of living and fossil plants (Kenrick plants (Kenrick & Crane 1997a).A consequence of these& Crane 1997a,b; Mishler & Churchill 1984, 1985; life cycle differences is that sporophyte characteristicsfigure 1) and studies that have integrated morphology cannot be polorized in basal land plants. One approachwith data on 18S and 26S rRNA sequences (Mishler et al. to addressing these problems is to add aditional data (Poe 1994). However, the chloroplast gene rbcLfavours a horn- & Swoffiord1999), and there is evidence that combiningwort + vascular plant clade (Lewis et al. 1997). Both data from diffierentmolecular studies will provide a morehypotheses are consistent with the distribution of three robust solution (Mishler et al. 1994; Nishiyama & Katomitochondrial group II introns sampled across a wide 1999). A second approach is to add additional taxa and torange of land plants (Qiu et al. 1998).These data support break up long branches (Swoffiord al. 1996).This would etthe hypothesis that liverworts are either a sister group to be achieved most effiectivelythrough the better documen-all other land plants or perhaps a basal paraphyletic tation of fossil bryophytesfrom the Palaeozoic.assemblage. A third pattern resolves vascular plants as asister group to a moss + liverwort clade. This hypothesis (b) Rhyniophytes and basal vascular plantsis consistent with evidence from male gamete develop- There is almost universal support for monophyly of thement and ultrastructure (Garbary & Renzaglia 1998), as vascular plants crown group (i.e. the clade containing allwell as analyses based on gene sequencesfrom the nucleus living species: euphyllophytes + lycophytes; figure 1). (18S rRNA; Hedderson et al. 1996) and the mitochon- Moderate to high bootstrap support has been reporteddrion (19Sr DNA; DuS & Nickrent 1999). This pattern from the analysis of 18S rRNA (Hedderson et al. 1998;also receives support from a recent analysis based on Kranz & Huss 1996), and the mitochondrial l9S rDNAseveral plastid genes (rbcL,psaA, psaB, psbD, rpoCM, (Duff & Nickrent 1999) and cox3 (Malek et al. 1996)Nishiyama & Kato 1999). genes. Monophyly is supported by data on the ultra- Support for these hypotheses, as measured by bootstrap structure and development of the male gamete (Garbaryand decay indices, is generally comparatively low, and & Renzaglia 1998) and from general comparativealternative topologies are only marginally less parsimo- morphology (Kenrick & Crane 1997a; Stevenson &nious. Based on mitochondrial cox3sequences, Malek et al. Loconte 1996). Analyses based on the chloroplast gene (1996) resolved hornworts as basal in embryophytes, but rbcL do not resolve vascular plants as monophyleticthe relationshipsof liverworts, mosses and vascular plants (Manhart 1994). The rbcL-based analyses, however,had very low support. Data on spermatogenesis and provide highly incongruent results with little bootstrapsperm ultrastructureindicate that bryophytes are mono- support among basal groups. It seems likely that thephyletic (Garbary et al. 1993; Maden et al. 1997), but noise-to-signal ratio for rbcL is extremely high at thissampling is comparatively sparse and there is concern level in land plants (Manhart 1994).about character independence in some data domains (e.g. Inclusion of fossils indicates that the extinct Rhynio-the ultrastructure of the spermatozoid flagellum). phytina (Banks 1992; Edwards & Edwards 1986) are aRecoding of the Garbary et al. (1993) data by Mishler grade of organization comprising stem group vascularet al. (1994) and Garbary & Renzaglia (1998) produced plants (protracheophytes) as well as probable basala tree topology that is consistent with bryophyte members of the crown group (Kenrick & Crane 1997a;paraphyly. figure 1). Monophyly of the stem-based group is supported The absence of consensus among data sets and the in morphological cladistic analyses, indicating that struc-generally low levels of support for alternativephylogenetic tures such as the tracheid are homologous in vascularhypotheses are most likely a consequence of several plants. Marginally less parsimonious topologies would beproblems that emerge at this phylogenetic level in plants. consistent with the rooting of certain bryophyte groupsFirst, the cladogenic events that led to the evolution of within the vascular plant stem-based group (figure 1). Inthese groups occurred between 470 and 400 Myr ago other words, the evolution of mosses from protracheo- (Kenrick & Crane 1997b).The interval of time spanning phytes through, among other things, loss of sporophytegroup divergence is short in comparison with the length branching is consistent with trees three steps longer thanof time between these events and the present. In other the most parsimonious tree. Note, however, that this typewords, phylogenetic methods are likely to perform poorly of relationship is also consistent with monophyly of thebecause of imbalance in branch length (i.e. short internal vascular plant crown group and is thereforedetectableonlybranches combined with long terminal branches, see in analyses that include fossils (Kenrick & Crane 1997a).Felsenstein 1978; Huelsenbeck 1995). Second, the greatdiffierencesbetween comparable phases of the bryophyte (c) Lycophytes and euphyllophytesand vascular plant life cycle create difficulties in identify- In vascular plants, the weight of evidence froming homologies for morphological analyses. The absence comparative morphology, gene sequences and data onof a fossil recordof stem group mosses,liverwortsand genome structure favours lycophytes as sister group to ahornworts exacerbatesthis problem(Kenrick& Crane clade comprisingall other living vascular plants (euphyllo-1997a).Third,in morphological rootingthe tree analyses, phytes; figure 1). Lycophytes are consistently resolved asand characterpolarity are problematic because of the sister group to euphyllophytes based on nuclear (18Scomparatively large gap between land plants and their rRNA, Kranz & Huss 1996) and mitochondrial (19S Lond.B (2000)Phil. Trans. SOG. R.
850 P. Kenrick RelationshitsofrascularplantsrDNA, DuS & Nickrent 1999; cox3, Malek et al. 1996) (Kenrick & Crane 1997a). Controversially, Rothwellgene sequences. The euphyllophyte clade is also strongly (1996) found cladoxylopsids and zygopterids to be morecorroborated by a 30 kb inversion in the chloroplast closely related to seed plants than to either ferns or Equi-genome, which is absent from lycophytes and liverworts setum. The prospects of resolving this issue are compara- (Raubeson & Jansen 1992). Furthermore,there is strong tively good, because of the excellent fossil record of thesesupport from comparative morphology for this topology, groups. Furtherdetailed work on the morphology of Lateparticularly from studies that include fossils (Kenrick & Palaeozoic plants is required, in particular the recon-Crane 1997a,b;Stevenson & Loconte 1996). struction of whole plants. Conflicting data from other gene sequences generallyexhibit low bootstrap support on the critical basal (d) Theproblematic Psilotum and Tmesipterisbranches and they are mutually contradictory.The rbcL One group that figures prominently in higher-levelgene resolves lycophytes as sister group to seed plants phylogenetic studies of vascular plants is the Psilotaceae:(Manhart 1994;Wikstrom & Kenrick 1997), but support a group comprising some 15 species of fern-like plantsfor this relationship and consistency indices are very low. classified into two genera, Psilotum and Emesitteris.Psilo-In an analysis of relationships among pteridophytes, the taceae are problematic, and in the recent literature therechloroplast atpB sequence resolved lycophytes as poly- have been two very diffierentinterpretations of the rela-phyletic (Wolf 1997).This result is highly unparsimonious tionships and hence the evolution of the group. Thewith respect to comparative morphology and is not problem revolves around how to interpret the simplesupported by other molecular data. Selaginella placed was sporophyte and gametophyte morphology.The simplicitysister group to all other vascular plants, but Huterziaand of these plants has been interpreted as plesiomorphic andIsoetes grouped within ferns. Combining atpB and rbcLfor they have been compared with the simple sporophytesofpteridophytesplaced Selaginella within ferns, and a Huterzia early fossil vascular plants (e.g. Rhynia).Under this + Isoetesclade as sister group to ferns (Wolf 1997). In hypothesis, these relicts from the Devonian Period shouldview of the behaviour of lycophytes in rbcL data sets, emerge as sister group to all other vascular plantsinclusion of seed plant sequencesin this combined analysis (Bremer 1985).However, Gensel (1977, 1992)has pointedmay well have had a significant affiecton tree topology. out that there are few unequivocal characters linking Relationships among basal living and fossil euphyllo- Psilotaceae to rhyniophytesor trimerophytes.An alterna-phytes are still rather poorly resolved. Living groups such tive hypothesis views the morphological simplicity ofas leptosporangiate ferns, Ophioglossales, Marattiales, Psilotaceae as a product of reduction, perhaps related toEquisetumand seed plants are clearly monophyletic the epiphytic habit, which is typical of many species.(Doyle 1998; Kenrick & Crane 1997a; Pryer et al. 1995; Based on a detailed comparative study of gametophyteRothwell & Serbet 1994; Vangerow et al. 1999), but the and sporophyte Bierhorst (1977)argued that Psilotaceaebootstrap support for relationshipsamong these groups in are closely related to leptosporangiate ferns, specificallysequence-based studies is generally low (DuS & Nickrent Stromatopteris (Gleicheniaceae). Although aspects of this1999; Hedderson et al. 1998; Kranz & Huss 1996; Malek hypothesis have been criticized, in particular the formula-et al. 1996; Pahnke et al. 1996; Pryer et al. 1995;Wolf 1997) tion of homologies in the stem/leafsystem (Kaplan 1977),and critical taxa are frequently missing. No consistent there are similarities between Psilotaceae and severalpattern has yet emerged. DuS & Nickrent (1999) resolved basal groups in ferns in general (Kenrick & Crane 1997a;a well-supported fern + Equisetum clade as sister group to Pryer et al. 1995;Stevenson & Loconte 1996).Molecularseed plants, in agreement with one fossil-based cladistic data provide compelling evidence that Psilotaceae areanalysis (Kenrick & Crane 1997a). But the sample of related to basal euphyllophytes. Psilotaceae share a 30 kbleptosporangiate ferns was based on a single species of inversion in the chloroplast genome that is unique to thePolypodium, Marattiales and Psilotum and were absent from euphyllophyte clade (Raubeson & Jansen 1992). 18Sthe analysis. The basal groups of living euphyllophytes rRNA sequences group Psilotum basal euphyllophytes inare morphologically quite divergent, and phylogenetic (Kranz & Huss 1996).More specifically, a close relation-studies based on the comparative morphology of living ship between Psilotaceae and Ophioglossales is supportedspecies show that there are comparatively few character- by data from three chloroplast gene sequences (rbcL,istics supporting tree topology (Stevenson & Loconte Manhart 1994; 16S rDNA, Manhart 1995; atpB,Wolf1996).This study placed Equisetum sister group to a clade 1997)and the mitochondrial cox3 (Malek et al. 1996)andcomprising leptosporangiate ferns, eusporangiate ferns nadS genes (Vangerowetal. 1999).and seed plants, a result that is consistent with at leastone cladistic analysis that includes fossils (Rothwell 1996). 3. VASCULARPLANTSAS BRYOPHYTES Consideration of fossil evidence from the Late Palaeo-zoic underlines further basic similarities among these Even though many details of land plant phylogenydiverse living groups.The seed plant stem group contains remain unresolved, it is clear that bryophytes andplants (progymnosperms) with some of the wood and vascular plants are very closely related indeed. Thebranching characteristicsof seed plants, but which retain weight of evidence favours a single origin of land plantsthe plesiomorphic free-sporing life cycle. Other key fossil and implies that vascular plants arebryophytes with agroups include cladoxylopsidsand zygopterids.These two highly modified life history. This result has far-reachinggroups are widely thought to be related to ferns and Equi- consequences for interpreting land plant morphology. Itsetum, although the precise nature of this relationship implies that the major features shared by most land plantsremains unresolved (Stein et al. 1984). One fossil-based (e.g. multicellular gametangia, diplobiontic life cycle,cladistic analysis has found support for this hypothesis stomates, sporangium) originated from a commonPhzl.Trans. SOG. R. Lond.B (2000)
Relationshitsofvascularplants P.Kenrick 851Figure2. Exceptionallywell-preserved silicifiedfossilgametophytes stemgroupvascularplantsfromthe 400 Myr old ofRhyniechert,Scotland(courtesy Remy and H. Hass,Westfalische W. Wilhelms-Universitat, Munster).(a) Terminalpartofgametophytic of Lyonophyton axis rhyniensis comprising slenderaxis (lowerpair arrows)terminating expandedgametangiophore in(upperpair arrows)(scale= 1mm). (b) Detailsof uppersurfaceof gametangiophore from (a) bearingspherical antheridium(arrow)(scale= 500,um).(c) Transversesectionof antheridium L. rhyniensis of showingdetailsof spermatidmothercells(scale= 100,um).(d) Archegonium Langiophyton showingneck (arrows, and egg chamber(arrow,e) (scale= 100,um). of mackiei n)ancestor and that any differences observed today are the phyte sporophytes are of a similar size and level of tissueresult of divergent evolution. In other words, similarities differentiation to the larger mosses. Other similaritiesamong major groups are not the result of convergence on include the absence of leaves and the presence of simplea similar set of adaptations to life on land, rather they terminal sporangia (Edwards 1993, 1996; Edwards et al.result from a common ancestry. We should therefore 1995; Fanning et al. 1992).With these data in mind, it isexpect substantial similarities at the molecular develop- possible to recognize several key developments that weremental level between organ systems in bryophytes and prerequisiteto the divergence and subsequentdiversifica-their homologues in vascular plants (Kenrick & Crane tion of the vascular plant sporophyte: (i) the development1997b). This prediction is currently untested. of apical growth leading inevitably to indeterminate Among living plants, life cycles have been used as a growth, sporophytic branching and the multiplication ofbasis for distinguishing vascular plants from bryophytes, parts; (ii) escape from nutritional dependence on thebut this clear distinction breaks down in the early fossil gametophyte (loss of sporophytic parasitism); and (iii)record. The diploid (sporophyte) phase of the vascular differentiationof various tissue systems for biomechanicalplant life cycle is much more highly differentiated and support (Kenrick & Crane 1997a,b; Niklas 1994, 1997;larger than the equivalent phase in liverworts and mosses. Speck & Vogellehner 1991,1994).The origin of these differences can be traced through a In contrast to the sporophyte, the haploid (gameto-series of extinct morphological intermediates (Kenrick phyte) phase of the vascular plant life cycle is much1994; Remy et al. 1993; Remy & Hass 1996). Palaeo- smaller and generally less well-differentiated than thebotanical data show that the early vascular plant sporo- equivalent phase in bryophytes. In seed plants, the game-phytes resemble much more closely the bryophyte model tophyte is minute, and it is nutritionallydependent on the(Edwards et al. 1995;Raven 1985, 1993, 1995).Protracheo- sporophyte. In some groups of ferns and fern allies, it isPhil. 7Trans. Soc.Lond.B (2000) R.
852 P. Kenrick Relationshipsofrascularplants moss Huperzla Ophioglossum Aglaophytont Nothia t sf (2n) (iD (n) (n) (2n) (n) (2n) (n) (2n) l l l l lFigure 3. Hypothesis of life cycle evolution in basal vascular plants. t = extinct taxon. Evidence from phylogeny and the fossilrecord indicates that the vascular plant life cycle evolved from a bryophytic life cycle in which the sporophyte (2n) is parasitic onthe gametophyte (n). There was a transitional phase (now extinct) in which the life cycle was more or less isomorphic (hererepresented by the extinct plants Aglaophyton Aothia). The gametophytes of modern vascular plants are highly reduced, but andgroups such as Lycopodiaceae (Huperzia)and Ophioglossales (Ophioglossum) retain vestiges of this earlier morphologicalcomplexity (see Kenrick 1994).subterranean and saprophytic; in others, it is photo- with the phylogenetic tree, the fossil record or perhapssynthetic. In many ferns, the gametophyte is thalloid, both (Smith 1994).The paraphyleticrelationship of bryo-whereas in some it resembles a branched axis, and in phytes to vascular plants implies that the earliest landothers it is more or less disc-shaped with a peculiar ring plants were bryophyte-like organisms. Therefore, themeristem. The origin of these differences has never been sequence of appearance of groups in the fossil recordfully explained. should show bryophytes preceding vascular plants. This New evidence from the fossil record is beginning to pattern is consistent with microfossil evidence (dispersedshed light on the origin of the gametophyte phase of the spores) but it conflicts with the megafossils (Kenrick &vascular plant life cycle. Recent discoveries document Crane 1997a,b).comparatively large and highly differentiated gameto- Fossil spores document a Mid-Ordovician origin ofphytes in early vascular plants and protracheophytes land plants (ca. 476 Myr) and a major diversification(Kenrick 1994; Remy et al. 1993; figure 2a-d). Although during the Late Ordovician and Silurian (Gray 1985,completely lacking leaves, perhaps the closest modern 1993;Wellman 1993, 1995, 1996;Wellman & Richardsonanalogue for these plants would be the larger moss game- 1993). Although the affinities of the early spore producerstophytes in the Polytrichales. This new fossil evidence are controversial, there is mounting evidence from laterimplies that vascular tissues and stomates have been lost spore/megafossil associations (Edwards et al. 1995;in the gametophytes of living vascular plants. Likewise, Fanning et al. 1991;Wellman et al. 1998), spore wall ultra-gametophyte branching and gametangiophore develop- structure (Taylor 1996) and fossil cuticles (Kroken et al.ment has been much reduced or lost completely. In other 1996) that they were produced by plants at the bryophytewords, the morphology of the gametophyte generation in grade. The spore evidence is thus consistent with theliving vascular plants is the product of extensive loss or results of phylogenetic analysis. Megafossils, on the otherreduction, which has probably occurred independently in hand, show a completely diffierentpattern. Their strati-several lineages. Most unexpectedly, the transition from graphic appearance is the reverse of that predicted bygametophyte-dominated to sporophyte-dominated life cladogram topology and it substantially postdates thecycles in land plants involved a now extinct isomorphic microfossil (spore) evidence (Kenrick & Crane 1997b).Inintermediate phase (figure 3), implying similar patterns the megafossil record, vascular plants and protracheo-of gene expression early on in both phases of the life phytes appear before bryophytes, and the diversificationcycle. of land plants apparentlybegins in the Mid-Silurian. Can these inconsistenciesbe reconciled? One source of potential error is the phylogenetic 4. IMPLICATIONS FOR LANDPLANTORIGINS analysis. Inverting relationships to place bryophytes The hierarchical structure of a phylogenetic tree within crown group vascular plants or deriving bryo-dictates a logical sequence to clade formation that can be phytes independently from other later algal groups wouldcompared with the actual pattern of appearance of be more consistent with the stratigraphic appearance ofgroups in the fossil record (see Norell & Novacek 1992; megafossils. But these solutions are highly unparsimo-Siddall 1998; Smith 1994). The phylogenetic and strati- nious. Furthermore,the inversion of relationships wouldgraphic approaches provide essentially independent esti- leave the early fossil record of bryophyte-like spores un-mates of the sequence in which events occurred. Because explained. A second and more likely source of error is acongruence between the results of these two processes is systematic representationalbias in the megafossil recordexpected, any deviation indicates that there is a problem favouring vascular plants over bryophytes. There arePhil. Wrans. SOG. R. Lond.B (2000)
Relationshipsofrascularplants Kenrick 853 P. the timing of these events. Recent phylogenetic results therefore corroborate earlier suggestions that the pattern of appearance and early diversification of plants in the megafossil record owes more to changing geological conditions than to rapid biological diversification (Gray 1985;Gray & Boucot 1977). I gratefully acknowledge a gift of transparenciesfrom W. Remy and H. Hass (Abteilung Palaobotanik am Geologisch-Palaonto- logischen Institut, WestfalischeWilhelms-Universitat, Munster, Germany), which form the basis of figure 2. Pollyanna Lidmark preparedfigures 3 and 4. REFERENCES Allen, J. R. L. 1985 Marine to fresh water: the sedimentology of the interrupted environmental transition (Ludlow-Siegenian) in the Anglo-Welsh region. Phil. Wrans. Soc. Lond. B309, R. 85-104. Banks, H. P. 1992 The classification of early land plants- revisited. In Proceedings the Birbal Sahni Birth Centenary of Palaeobotanical Conference, 22 (ed. B. S. Venkatachala, K. P. vol. Jain & N. Awasthi), pp. 49-63. Lucknow:The Palaeobotanical Society. Bierhorst, D. W. 1977 The systematic position of Psilotumand Tmesipteris.Brittonia 3-13. 29, Bremer,K. 1985 Summary of green plant phylogeny and classifi- cation. Cladistics 369-385. 1, Crowe, C. T., Pike, L. M., Cross, K. S. & Renzaglia, K. S. 1997Figure 4. Hypothetical stem group moss before the The psbA gene sequence can be used to infer phylogeneticevolution of gametophytic leaves. Small, unbranched, relationshipsamong the major lineages of bryophytes. Am.3.valvate sporophytes (s) with columella of Andreaea type Bot. 84, 14-15.attached terminally to naked, dichotomously branched Doyle, J. A. 1998 Phylogeny of vascular plants. A. Rev.Ecol.Syst.gametophyte (g). 29, 567-599. Duff, J. R. & Nickrent, D. L. 1999 Phylogenetic relationshipsofseveral observations that tend to favour representational land plants using mitochondrial small-subunit rDNAbias as an explanation for these inconsistencies. First, sequences.Am.3. Bot. 86, 372-386. Edwards, D. 1990 Constraints on Silurian and early Devonianbryophytes are generally rare in comparison with phytogeographic analysis based on megafossils. In Palaeozoicvascular plants throughout the pre-Quaternary fossil palaeogeography biogeography W. S. McKerrow & C. R. and (ed.record. This fact is probably related to their compara- Scotese), pp. 233-242. London:The Geological Society.tively small size, the absence of lignin and woody tissues Edwards, D. 1993 Cells and tissues in the vegetative sporophytes(low fossilization potential), and collector bias favouring of early land plants. JWewPhytol. 125, 225-247.vascular plants. Second, a search image based on modern Edwards, D. 1996 New insights into early land ecosystems: abryophytes is likely to be unproductive in the early fossil glimpse of a Lilliputian world. Rev. Palaeobot. Palynol.90,record. For example, leaves are a characteristicof modern 159- 174.moss gametophytes, but it is highly likely that stem group Edwards, D. & Edwards, D. S. 1986 A reconsideration of themosses were leafless (Mishler & Churchill 1984). Such Rhyniophytina Banks. In Systematic taxonomic and approaches in palaeobotany, vol. 31 (ed. R. A. Spicer & B. A. Thomas),leafless mosses would be difficult to recognize and to pp. 199-220. Oxford: Clarendon Press.distinguish from stem group vascular plants (figure 4). Edwards, D., Duckett, J. G. & Richardson, J. B. 1995 HepaticThird, the rapid appearance of megafossils in the Early charactersin the earliest land plants. J%ature 635-636. 374,Devonian coincides with major facies changes driven by a Fanning, U., Richardson,J. B. & Edwards, D. 1991A review ofwidespread marine regression in northern Europe, one of in situ spores in Silurian land plants. In Pollenand spores, vol.the major sampling areas (Allen 1985; Gray & Boucot 44 (ed. S. Blackmore & S. H. Barnes), pp. 25-47. Oxford: 1977).More generally, all Silurian land plant megafossils Clarendon Press.are from marine sediments, whereas Early Devonian Fanning, U., Edwards, D. & Richardson, J. B. 1992 A diverseplant localities are predominantly terrestrial (Edwards assemblage of early land plants from the Lower Devonian of 1990). In contrast to megafossils, the spores of bryophytes theWelsh Borderland.Bot.3. Linn.Soc.109, 161-188.and vascular plants are essentially equivalent in tapho- Felsenstein,J. 1978 Cases in which parsimony and compatibility methods will be positively misleading. Syst.Zool.27, 401-410.nomic terms. They are of similar size, composition and Garbary,D. J. & Renzaglia, K. S. 1998 Bryophytephylogenyanddispersal ability. Spores would therefore be expected to the evolution of land plants: evidence from development anddocument more accurately the composition of the terres- ultrastructure. In Bryology the twenty-hrst for century(ed. j. w.trial flora at this time. Spores are also vastly more abun- Bates, N.W. Ashton &J. Duckett). Leeds: Maney & Son. G.dant and more widely dispersed into a broader range of Garbary, D. j., Renzaglia, K. S. & Duckett, J. G. 1993 Thefacies (shallow marine, terrestrial) than are the megafos- phylogeny of land plants: a cladistic analysis based on malesils. They are expected to give a more complete picture of gametogenesis.Pl. Syst.Evol.188, 237-269.Phil. Wrans. Soc.Lond.B (2000) R.
854 P. Kenrick RelationshipsofrascularplantsGensel, P. G. 1977 Morphologic and taxonomic relationshipsof Mishler, B. D. & Churchill, S. P. 1985 Transitionto a land flora: the Psilotaceae relative to evolutionary lines in early land phylogenetic relationshipsof the green algae and bryophytes. vascular plants. Brittonia 14-29. 29, Cladistics 305-328. 1,Gensel, P. G. 1992 Phylogeneticrelationshipsof the zosterophylls Mishler, B. D., Lewis, L. A., Buchheim, M. A., ltenzaglia, K. S., and lycopsids: evidence from morphology, paleoecology and Garbary, D. J., Delwiche, C. F., Zechman, F. W., Kantz, T. S. cladistic methods of inference. Ann.Mo. Bot. Gdn79, 450-473. & Chapman, R. L. 1994 Phylogenetic relationships of theGray, J. 1985 The microfossil record of early land plants: greenalgaeand bryophytes. Ann.Mo.Bot.Gdn81, 451-483. advances in understanding of early terrestrialization, 1970- Niklas, K. J. 1994 Plant allometry: scalingofform andprocess. the 1984. Phil. Wrans. Soc.Lond.B 309, 167-195. R. University of Chicago Press.Gray, J. 1993 Major Paleozoic land plant evolutionary bio- Niklas, K. J. 1997 The evolutionary biology plants. University of of events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 153-169. 104, Chicago Press.Gray,j. & Boucot, A. j. 1977 Early vascular land plants: proof Nishiyama,T. & Kato, M. 1999 Molecular phylogenetic analysis and conjecture.Lethaia10, 145-174. among bryophytes and tracheophytes based on combinedHedderson, T. A., Chapman, R. L. & Rootes, W. L. 1996 data of plastid coded genes and the 18S rRNA gene. Mol. Biol. Phylogenetic relationships of bryophytes inferred from Evol.16, 1027-1036. nuclear encoded rRNA gene sequences. Pl. Syst. Evol. 200, Norell, M. A. & Novacek, M. L. 1992 Congruence between 213-224. superpositionaland phylogeneticpatterns:comparing cladisticHedderson, T. A., Chapman, R. L. & Cox, C. J. 1998 patternswith fossil records. Cladistics 319-337. 8, Bryophytes and the origins and diversificationof land plants: Pahnke, J., Goremykin,C, Bobrova,, Troitsky,A., Antonov, new evidence from molecules. In Bryology the twenty-first for A. & Martin, W. 1996 Utility of rDNA internal tran- century j. w.Bates, N. W. Ashton & j. G. Duckett), pp. 65- (ed. scribed spacer sequences from the inverted repeat of 77. Leeds: Maney & Son. chloroplast DNA in pteridophyte molecular phylogenetics.Huelsenbeck,J.P.1995 Performanceof phylogenetic methods in In Pteridology perspective J. M. Camus, M. Gibby & in (ed. simulation. Syst.Biol. 44, 17-48. R. J. Johns), pp.217-230. London: Royal Botanic Gardens,Kaplan, D. 1t. 1977 Morphological status of the shoot systems of Kew. Psilotaceae. Brittonia 30-53. 29, Pickett-Heaps,J. D. & Marchant, H. J. 1972 The phylogeny ofKenrick, P. 1994 Alternation of generations in land plants: new green algae: a new proposal. Cytobios 255-264. 6, phylogenetic and morphological evidence. Biol. Rev. 69, Poe, S. & Swofford, D. L. 1999 Taxon sampling revisited. J%ature 293-330. 398, 299-300.Kenrick, P. & Crane, P. R. 1997aTheoriginandeary diversification Pryer, K. M., Smith, A. R. & Skog, J. E. 1995 Phylogenetic of land plants: a cladistic study. Smithsonian Series in relationships of extant ferns based on evidence from Comparative Evolutionary Biology.Washington: Smithsonian morphology and rbcLsequences.Am.Fern3.85, 205-282. Institution Press. Qiu, Y.-L., Cho, Y., Cox, J. C. & Palmer,J. D. 1998 The gain ofKenrick, P. & Crane, P. R. 1997bThe origin and early evolution three mitochondrial introns identifiesliverworts as the earliest of plants on land. J%ature 33-39. 389, land plants. J%ature 671-674. 394,Kranz, H. D. & Huss, V. A. R. 1996 Molecular evolution of Raubeson, L. A. & Jansen, R. K. 1992 Chloroplast DNA pteridophytes and their relationshipsto seed plants: evidence evidence on the ancient evolutionary split in vascular land from complete 18S rRNA gene sequences. Pl. Syst.Evol. 202, plants. Science 255, 1697-1699. 1-11. Raven, J. A. 1985 Comparative physiology of plant andKranz, H. D., Miks, D., Siegler, M.-L., Capesius, I., Sensen,W. arthropod land adaptation. Phil. Wrans. Soc. Lond. B 309, R. & Huss,V. A. R. 1995 The origin of land plants: phylogenetic 273-288. relationships among charophytes, bryophytes, and vascular Raven, J. A. 1993 The evolution of vascular plants in relation to plants inferred from complete small-subunit ribosomal RNA quantitative functioning of dead water-conducting cells and gene sequences.J. Mol. Evol.41, 74-84. stomata. Biol. Rev.68, 337-363.Kroken, S. B., Graham, L. E. & Cook, M. E. 1996 Occurrence Raven, J. A. 1995 The early evolution of land plants: aquatic and evolutionary significance of resistant cell walls in charo- ancestors and atmospheric interactions. Bot. J. Scot. 47, phytes and bryophytes.Am.J. Bot. 83, 1241-1254. 151-176.Lewis, L. A., Mishler, B. D. & Vilgalys, R. 1997 Phylogenetic Remy, W. & Hass, H. 1996 New information on gametophytes relationships of the liverworts (Hepaticae), a basal embryo- and sporophytes of Aglaophyton majorand inferences about phyte lineage, inferred from nucleotide sequence data of the possible environmental adaptations. Rev.Palaeobot. Paynol.90, chloroplastgene rbcL.Mol. Phylogenet. 7, 377-393. Evol. 175-194.Maden, A. R., Whittier, D. P., Garbary,D. j. & Renzaglia, K. S. Remy, W., Gensel, P. G. & Hass, H. 1993 The gametophyte 1997 Ultrastructureof the spermatozoidof Lycopodiella lateralis generation of some early Devonian land plants. Int. J. Pl. Sci. (Lycopodiaceae).Can. Bot.75, 1728-1738. J. 154, 35-58.Malek, O., Lattig, K., Hiesel, R., Brennicke, A. & Knoop, V Rothwell, G. W. 1996 Phylogenetic relationships of ferns: a 1996 RNA editing in bryophytes and a molecular phylogeny paleobotanical perspective. In Pteridology perspective in (ed. of land plants. EMBOJ. 15, 1403-1411. J. M. Camus, M. Gibby & R. J. Johns), pp. 395-404. London:Manhart, J. R. 1994 Phylogenetic analysis of green plant rbcL Royal Botanic Gardens, Kew. sequences.Mol. Phylogenet. 3, 114-127. Evol. Rothwell, G. W. & Serbet, R. 1994 Lignophyte phylogeny andManhart, J. R. 1995 Chloroplast 16S rDNA sequences and the evolution of spermatophytes: a numerical cladistic phylogenetic relationships of fern allies and ferns. Am. FernJ. analysis. Syst.Bot. 19, 443-482. 85, 182-192. Siddall, M. E. 1998 Stratigraphicfit to phylogenies: a proposedMattox, K. R. & Stewart, K. D. 1984 Classificationof the green solution. Cladistics 201-208. 14, algae: a concept based on comparative cytology. In Systematics Smith, A. B. 1994 Systematics thefossilrecord: and documenting evolu- of thegreenalgae,vol. 27 (ed. D. E. G. Irvine & D. M. John), tionarypatterns. Oxford: Blackwell. pp. 29-72. London: Academic Press. Speck,T. & Vogellehner, 1991Biomechanics maximum D. andMishler, B. D. & Churchill, S. P. 1984 A cladistic approach to height of some Devonian land plants. In Palaeovegetational the phylogeny of the bryophytes.Brittonia 406-424. 36, development Europeand regionsrelevantto its palaeoforistic inPhil. Trans. Soc.Lond.B (2000) R.
Relationshitsofvascularplants P.Kenrick 855 evolution.Proceedings thePan-European of Palaeobotanical Conference Vangerow,S., Teerkorn, & Knoop, V 1999 Phylogenetic infor- T. (ed. J. Kovar-Eder),pp. 413-422. Vienna: Museum of Natural mation in the mitochondrial nad5 gene of pteridophytes: History. RNA editing and intron sequences.Pl. Biol. 1, 235-243.Speck, T. & Vogellehner, D. 1994 Devonische Landpflanzen mit Wellman, C. H. 1993 A land plant microfossil assemblage of und ohne hypodermales sterom-eine biomechanische Mid Silurian age from the Stonehaven Group, Scotland. 7. analyse mit uberlegungen zur fruhevolutiondes leit- und festi- Micropalaeontol. 47-66. 12, gungssystems.Palaeontographica B 233, 157-227. Wellman, C. H. 1995 Phytodebrisfrom Scottish Silurian andStein, W. E., Wight, D. C. & Beck, C. B. 1984 Possible alterna- Lower Devonian continental deposits. Rev. Palaeobot. Palynol. tives for the origin of Sphenopsida.Syst.Bot. 9, 102-118. 84, 255-279.Stevenson, D. W. & Loconte, H. 1996 Ordinal and familial Wellman,C. H. 1996Cryptospores fromthe type areaofthe Caradoc relationshipsof pteridophytegenera. In Pteridology perspective in Seriesin southernBritain.Spec. Palaeontol. 103-136. Pap. 55, (ed. J. M. Camus, M. Gibby & R. J. Johns), pp.435-467. Wellman, C. H. & Richardson, J. B. 1993 Terrestrial plant London: Royal Botanic Gardens, Kew. microfossilsfrom the Silurian Inliers of the Midland Valley ofStewart, K. D. & Mattox, K. R. 1975 Comparative cytology, Scotland. Palaeontology 155-193. 36, evolution and classification of the green algae with some Wellman, C. H., Edwards, D. & Axe, L. 1998 Permanentdyads consideration of the origin of other organisms with chloro- in sporangia from the Lower Devonian of the Welsh phylls A and B. Bot.Rev.41, 104-135. Borderland.Bot. 7. Linn.Soc.127,117-147.Swoffiord, L., Olsen, G.J.,Waddell, P.J. & Hillis, D. M. 1996 D. Wikstrom, N. & Kenrick, P. 1997 Phylogeny of Lycopodiaceae Phylogenetic inference. In Molecularsystematics (ed. D. M. (Lycopsida) and the relationships of Phylloglossum drummondii Hillis, C. Moritz & B. K. Mable), pp. 407-514. Sunderland, Kunze based on rbcLsequences.Int.3. Pl. Sci. 158, 862-871. MA: Sinauer. Wolf, P. G. 1997 Evaluation of atpB nucleotide sequences forTaylor,W. A. 1996 Ultrastructureof lower Paleozoic dyads from phylogenetic studies of ferns and other pteridophytes. Am. J. southern Ohio. Rev.Palaeobot. Palynol. 269-280. 92, Bot.84, 1429-1440.Phil. Wrans. SOG. R. Lond.B (2000)