An Essay on STOR Paleobotanical Phylogenetics

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Experimental Cladistic Analysis of Anatomically Preserved Arborescent Lycopsids from the Carboniferous of Euramerlca: An Essay on STOR Paleobotanical Phylogenetics

Richard M. Bateman; William A. DiMichele; Debra A. WiUard

Annals of the Missouri Botanical Garden, Vol. 79, No. 3 (1992), 500-559.

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http: //w w w .j s tor. org/ Wed Sep 1 12:57:06 2004 EXPERIMENTAL CLADISTIC Richard M. Ba^eman^^ ANAT YSTS OF WLlliam. A. DiMickete,^ and . ^» ~^^,,^ Debra. A. Willard^'- ANATOMICALLY PRESERVED ARBORESCENT LYCOPSIDS FROM THE CARBONIFEROUS OF EURAMERICA: AN ESSAY ON PALEOBOTANICAL PHYLOGENETICS^

ABSTRACT

This evolutionary cladistic analysis of the arborescent (wood-producing) lycopsids, an exclusively fossil group of vascular plants, is confined to the strongest available data: anatomically preserved fossils that have been painstakingly reconstructed into conceptual whole plants. Ten Carboniferous genera are represented by 16 species: four pseudoherbs/ *'shrubs" and 12 of tbe arboreous (tree-siaed) species that epitomize the Pennsylvanian coal swarnps of Euramerica- The 69 vegetative and 46 reproductive characters are described in detail; several key terms are redefined and homologies reassessed. Binary coding was imposed throughout the data matrix, which contained only 5% missing values despite limited X-coding. Laek of an acceptable outgroup necessitated constructiod of a hypothetical ancestor for character polarization and tree rooting. Our experimental approach analyzed tbe full data matrix plus four suhmatrices (growth habit characters excluded, Chaloneria excluded, vegetative characters only, reproductive characters only) and screened topologies of subminimal as well as minimal length. Interpretation focuses on the ten monophyletic genera and marginally favors tbe topology {{Paaradendron, Oxroadia) (Anabathra (Chaloneria (Sigiliaria {{Diaphjiradendron, SynchyiidendroTi) (ffizemo- dendroniLepidodendran, Lepidophloios))))))). Other parsimonious topologies allow dissociation of tbe Paur^dendron- Ojjroajiia clade (probably justified), transposition or unification of ^nafeo/A-ra and Chaloiisria, and addition olSigillaria to the Diaphorodertdron^Synchyaidendron, ctade. The analysis confined to vegetative characters translocates Hiz~ em/idendron close to the base of the clade, thus unldng the non-trees as an ostensibly parapbyletic basal group. The analysis confined to reproductive characters more closely resembles the analysis of all characters, butufails to resolve relationships among the four basal, bisporangiate-coned genera, and between Hiz^modendron and Lepidodendron. These observations cast doubt on the value of partial-plant and isolated-organ phylogenies. Parsimonious use of the increasingly sophisticated and ff-selected reproductive strategies as the basis of the overall phylogeny inevitably renders homoplastic the partly discordant vegetative architectures (including the tree habit). Consequently, a poorly resolved parapbyletic plexus of four primitive, bisporangiate-coned genera (Patirodetidran, Oxroadia, Anabathra, Chaloneria) subtends a monophyletic monosporangiate-coned clade of three well-supported, monophyletic families: the SigiUariaceae (Sigiiiaria) are primitive relative to the Diaphorodendraceae {DiaphoToden- dron sens, str., Sym^kysidendron) and the Lepidodendraceae (Hizemodendron, Lepidad^ndron sens, str., Lepido- phloios), which together are characterized by a single functional raegaspore per megasporangium. This apparently progressive evolutionary trend toward seedlike reproducdon increased ecological specialization and is consistent with adaptive scenarios. In contrast with reproductive features, vegetative features such as the determinate growth, centralized rhizomorphic rootstock, and small number of module types that constitute the bauplan (rhizomorph and stem essential, lateral and crown branches optional) apparently predisposed the arborescent lycopsids to nonadaptive saltational evolution. Mutation of genes controlling early development allowed radical changes in growth architecture, and consequent

' We thank J. A. Coddington and R. A. Gastaldo for official reviews and J. I. Davis and R. Mooi for unofficial reviews. We also thank J. Clark, L. M. McCook, G. Paulay, and K. B. Pigg.for critically reading the manuscript, and J. Alroy for access to his unpublished software. M. Parrish kindly prepared final drafts of the diagrams. R Bateman acknowledges the support of the English-Speakir^ Union of the Commonwealths' Lindemann Trust Researcl. Fellowship, together with the Smithsonian Institution's "Evolution of Terrestrial Ecosystems" program. W. DiMicheU laid the foundations for this study while supported by NSF grant BSR 8210475. D. Willard acknowledges receipt o[ a Smithsonian Institution post-doctoral research fellowship. Errors and eccentricities are the authors' own. 'Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C 20560, U.S.A. •' Present address: Departments of Earth and Plant Sciences, University of Oxford, Parks Road, Oxford 0X1 3PR U.K. ' Present address: United States Geological Survey, 970 National Center, Reston, Virginia 22092, U.S.A.

ANN. MISSOURI BOT. GARD. 79: 500-559. 1992. Volume 79, Number 3 Bateman etal. 501 1992 Arborescent Lycopsid Phylogeny

epigenetic readjustment and adaptive honing affected many other vegetative characters. The progenctic (heterochronic) origin postulated for the pseudoherb Hiz^modsndroii may also apply to Ckaloneria and the other pseudoherhs (Paarodendron, Oxroadia), arguably comprising their value in scoring habit characters for the hypothetical ancestor. Other limitations of the present data matrix are the large number of genus-level autapomorphiea (at least partly reflecting the absence of pre-Pennsylvanian arboreous species), the inclusion of only one biaporangiate-coned tree (Anahathrd) and of only one putative isoetalean (Ckaloneria). More primitive OTUs are needed to investigate the origins of profound character states shared by all OTUs in the present study (e.g., secondary thickening, determinate growth, centralized rhizomorph, heterospory), and to confirm the crucial hypotheses of monophyly for the monosporangiate cone and the single functional njegaspore. Repeated simplification of growth architecture by progenesis and of megaspore ornamentation by functional redundancy show that evolution did not consistently increase morphological complexity among the arborescent lycopsids. Synapomorphies of highest burden (and therefore lowest homoplasy) tend to represent features of intermediate scale. We have not identified any significant drawbacks of cladistically analyzing an exclusively extinct set of OTUs. Rather, we recommend further study of some under-researched aspects of phylogeny reconstruction in general: (1) the effect of missing values on tree length calculations and on character state optimization; (2) the minimum acceptable level of empirical support (apomorphic states per OTU); (3) means of recogniiing heterochrony in cladograms; and (4) less methodologically constrained phonetic adjuncts to strict cladistic analyses.

Coal-swamp floras from the Peiuisylvamaii of alleled by increased knowledge of ontogeny (Wal- Euramerica have remained the most intensively ton, 1935; Eggert, 1961; Chaloner & Meyer-Ber- investigated and best known.flf aU Paleozoic plant thaud, 1983; Phillips & DiMichele, 1992) and communities throughout the last two centuries of reproductive biology (e.g., Thomas, 1978, 1981; detailed scientific study. Their popularity largely Phillips, 1979). reflects the unu.sual abundance of spores, adpressed Earlier higher classifications of the arborescent megafossQs, and anatomically preserved megafos- lycopsids focused on ostensibly well-known genera sds in these depositional environments and the eco- such as SLgUlaria, Botkrodendron, Lepidopkloi- nomic importance of coal (e.g., Scott, 1987). Stud- os, and 'Lepidodendron.'' sens. lat. and remained ies of permineralized coal-baU floras (e.g., Scott & fairly stable throughout much of this century (see Rex, 1985) have been especiaQy important in pro- Chaloner, 1967, for the most detailed account). viding detailed iriformatioii on the morphology and More recently, these conventional supraspecific anatomy of the plants that comprised the coal- classifications have been challenged. Thomas & swamp communities (e.g., Taylor, 1981; Stewart, Brack-Hanes (1984) devised a controversial sys- 1983; Bateman, 1991b; DiMichele et al., 1992). tem of satellite taxa that more accurately reflects Early workers (e.g., Grand'Eury, 1877; William- the variable and fragmentary nature of the paleobo- son, 1893; Scott, 1908; Seward, 1910) soon rec- tanical data, albeit at the expense of emphasizing ognized that the majority of the coal-ball floras reproductive structures rather than whole plants. were of low diversity and dominated (both in terms Using a contrasting philosophy (but generating an of body size and biomass) by trees that exhibited equally controversial result), DiMichele (1979a, b, clear morphological (and, by inference, phyloge- 1980, 1981, 1983, 1985) revised several arbo- rvetic) similarities to an extant group of ecologically rescent lycopsid genera as part of a program of insignificant, exclusively herbaceous, free-sporing whole-plant reconstruction, implicitly intended to plants, the lycopsids or *'clubmosses" (see Appen- delimit potentially monophylefic taxa within Lep- dix lA for discussion of the nomenclature and idodendron. sens. lat. This revision has been ex- systematics of higher taxa). tended by Bateman & DiMichele (1991) and The fossil tree-lycopsids occur un a severely dis- DiMichele & Bateman (1992). articulated condition, and must bp painstakingly We believe that sufficient credible whole-plant reconstructed if they are to be understood aa bi- reconatructiorija of arborescent lycopaida are now ological entities. Some early speculative restora- avadable (Figs. 1, 2) to allow explicit phylogenetic tions of these plants were remarkably accuraite analysis, using cladistic methods. To date, cladistic (e.g., Grand'Eury, 1877). Recently, more rigorous analysis has been appUed sparingly to long-extinct reco/istriicfio/is (DiMichele, 1979a, b, 1980, 1981, (i.e., paleobotanical) species, which have invariably 1983, 1985; DiMichele & PhilUps, 1985) have been admixed with their extant putative descen- been achieved using evidence of organic connection dants. Most of these studies focused •an seed plants supported by quantified association/dissociation (Hill & Crane, 1982; Crane, 1985a, b; Doyle & values (e.g., Bateman & RothweU, 1990) and par- Donoghue, 1986a, b, 1987a, b; Donoghue & Doyle, 502 Annals of the Missouri Botanical Garden

torical relationships of various arborescent lycopsids. We chose to analyze our data within the now well-estabUshed framework of evolutionary cladistics (e.g., WQey, 1981; Farris, 1983; Funk & Brooks, 1990; WQey et al., 1991) in order to test scenarios concerning patterns and underlying mechanisms of evolution within the group. In particular, we wished to assess preconceived hypotheses concerning the phylogenetic distributions, functional roles, and ecological significance of aspects of growth architecture and reproductive biology. The structure and content of this paper reflect the philosophical framework outlined by Neff(1986) and elaborated by Bryant (1989). Bryant (1989, fig. lb) emphasized the creative, deductive nature of a priori character analysis and a posteriori phylogenetic interpretation relative to the purely syn- thetic, empirical, inductive procedure of tree construction. Our phylogenetic analysis investigates aU three of these phases in detail, attempting to exploit the main benefit of cladisticsi'conceptual and methodological explicitness.

SELECTION AND PARTITIONING OF WHOLE-PLANT SPECIES

In order to qualify for inclusion in this study, plants had to be (I) either members of potential outgroups of the Order Lepidodendraj;gs (lycopsids possessing rhizomorphs, secondary thickening, periderm, ligules, and heterospory; Stewart, 1983), FIGURE 1. .Reconstructions of tree lycopaids, listed (2) anatomically preserved, and (3) known in suf- from left to right: DUipkaradendron sclerottciim (modi- ficient detail that aU disarticulated component or- fied after Wtiuk, 1985, fig. 19), LepLdophkios kalUi gans could be reconstructed to form a conceptual (modified after DiMichele & Phillips, 1985, fig. 2), An- whole plant (Chaloner, 1986; Bateman & Rothwell, abatkro. paUkerrima (redrawn from DiMichele & Phil- lips, 1985, fig. 2), Synckysidendron dicentrii^um. (mod- 1990; Bateman, 1991a); only whole-plant species ified after Wnuk, 1985, fig. 19), SLgillaria approximaia. can be thoroughly characterized. In practice, these (modified after Hirmer, 1927, fig. 284, and Stewart, three prerequisites confined our study to the Car- 1983, fig. 11.19). Diapliorodendran. pkillipsLi, Lepi- boniferous of Euramerica (Fig. 3), specifically to dodendron. hickii (after Wniik, 1985, fig. 12, and Tho- two species of Oxroadia from Mississippian vol- mas & Watson, 1976, textual description). All x 0.003. canigenic terrains (Bateman, 1988, 1992) and 15 species of nine genera (Appendix IC) from Penn- 19893, b; Donoghue, 1989; see also Hill & Camus, sylvanian coal swamps (e.g., Hirmer, 1927; Phil- 1986, on raarattialean "ferns"). Coticeptually, our lips, 1979; DiMichele & Phillips, 1985). (We have study owes much to Doyle & Donoghue (1986b) deliberately avoided formal reclassification in this in particular, but differs from all the above studies paper, though several recommendations for taxo- in focusing on relationships of taxa within a widely nomic revision are outlined in Appendix IC. Papers accepted order (Class Lycopsida, Order Lepidoden- derived from this study segregated Hizemoden- drales) that may lack extant descendants; certainly, dron from Lepidodendrort sens. str. (Bateman & all of the genera analyzed are extinct. The lycopsids DiMichele, 1991) and Synchysidendron, from are of particular phylogenetic interest as a potential Diapkorodendron, as well as erecting the new sister group of the remainder of the tracheophyte family Diaphorodendraceae (DiMichele & Bate- clade (Doyle & Donoghue, 1986b, fig. 1; Di- man, 1992). Our use of the generic name An.O' Michele & Skog, 1992). bathra rather than Paralycopodites follows Pear- Our purpose was not merely to unravel the his- son (1986) and is justified in Appendix IB). Volume 79, Number 3 Bateman et al. 503 1992 Arborescent Lycopsid Phylogeny

FIGURE 2. Reconatructiona of small-bodied lycopsids. —a. Hizemodendron serratum. —b. ChaUineria coriTiosa (redrawn from Pigg & Rothwell, 1983a, fig. 1).—c. Paarod^ndron. fraipontii (rtdrav/n from Schlanker & Leisraan, 1969, fig. 13).—d. OxToadLa gracilis (modified after Batematj, 1988, fig. 7.11). Aspects of the Hizemad^ndron reconstruction in particular are speculative, and it is more appropriately deacrilned as a restoration (Bateraan & DiMichele, 1991). a, b = x0.03, c, d - xO.I2,'

These conceptual whole-plant species of arbo- one whole-plant species (i.e., form-species sensu rescent lycopsid are listed in Table 1, together with Bateman & Rothwell, 1990; an organ whose mor- thehihliographicsourcesof much of onr data. Each phological expression is indistinguishable in two or conceptual whole plant encompasses at least nine more whole-plant species). Confining our study to readQy distinguiished organs (rootlet, rhixomorph, anatomically preserved material avoided the fur- stem, branch, leaf, megasporophyU, megaspore, ther complication of correlating the same organs microsporophyll, microspore) that are formally of the same whole-plant species in different pres- named, either individually or in aggregates, as or- ervation states (e.g., Galtier, 1986; Bateman, gan-species. Table 2 correlates the more important 1991a). of the organ-species that h^ve heen awarded Lin- Evidence for the reconstruction of these organ- nean binomials. Some organ-species binomials en- species into whole-plant species can be ascribed to compass more than one organ, most of the larget- three main categories (in order of increasing prob-, bodied whole-plant species encompass five named ability of correct correlation): as social ion/dissoci- organ-species (rootlet/rhizomorph, stem/branch/ ation (co-occurrence in space and time), anatomical leaf, strobilus/megasporophyll/microsporophyll, similarity, and organic connection {this has tradi- megaspore, microspore) and the smaller-bodied four tionally been regarded as proof of successful re- (rootlet/rhizomorph is not nomenclaturaUy distin- construction, though Bateman & Bothwell (1990) guished from stem/branch/leaf). Other binomials argued that at best it constitutes only a strong are applied to homologous organs of more than hypothesis). In practice, anatomical similarity is 504 Annals of the Missouri Botanical Garden

BHKIUITIAH PN AN Si DI/SY HZ/LN LS V3 ASBIW ?• V° V= HOLXERIAN X^ LU

ARUH[HAN X^

ChUOIAN

2 Tn3 • • i jvoniAN +^

MASTiWWl ?x^ x' ? Tni

FiCURE 3. Reported time rangea of OTUs (see caption to Table 3 for key to abbrevLationa). In general, last appearances are more reliable than first appearances. Inset shows first recorded occtirrences of the" genera (x = vegetative remains only, + — reproductive remains only, * — vegetative and reproductive remains). Superscripts denote bibliographic sources; Montagne Noire, south-central France: Rowe & Galtier, 1939, BatSman, 1992 (I), Meyer-Bert baud, 1984 (2); Burnmouth, northeastern England: Long, 1964 (3), Long, 1968 (4); Glenarbuck, southwestern Scotland: Smith, 1962 (5), Smith, 1962, 1964 (6); Laggan, Arran, southwestern Scotland: Fry, 1954 (7), Walton, 1935, Scott, 1990 (8); Pettycur, southeastern Scotland: Williamson, 187-2, 1393, Scott, 1900, 1920, Gordon, 1910, longmans, 1930, DiMichele, 1980, Pearson, 1986 (9), Benson, 1908 (10), Scott, 1901, Gordon, 1908 (11); Kingswood, southeastern Scotland: Scott et al., 1936 (12) (see also Scott et al, 1984). Time scale follows Leeder (1988). ' FlenLiagites ickopfii cone. ' F. diversm cone. usually employed in conjunc^tion with association/ giate cone (cf. Baxter, 1965; Leisman & Rivers, dissociation, and both are used as an adjunct to 1974; Batetnan & DiMichele, L991), and Sigil- organic connection, especially when attempts to laria "sp. nov.," which is strictly a Westphalian reconstruct whole plants by organic connection are A composite from more than one locality. only partially successful. In the case of our tree- It should be emphasized that the inevitable dis- lycopsids, organic connection is particularly diffi- articulation of their constituent individual organ- cult to demonstrate between reproductive organs isms into organ-aggregates or single organs renders and vegetative axes. It is easier to achieve cor- the reconstructed whole-plant species both con- relations between different organs within these two ceptual and typological. Each species is conceptual main categories; for example, by extracting in situ in the sense that it is a summation of several megaspores and microspores from cones (e.g., Tho- probabilities of correlation of pairs of organs rather mas, 1987; Willard, 1989a, h). Additional infor- than an integral, demonstrable fact. It is typological mation acquired since our analyses were performed in the sense that intraspecific variation can only suggests a closer relationship between Lepido- be documented among different specimens of the pkloias jokasonii and L. halUi. Otherwise, the same organ; complete data sets cannot be compiled least conclusive reconstructions in our analysis are for specific individuals, in contrast with morpho- Hizemodendroa serratam, where doubts surround metric studies of extant plants (e.g., Bateman & its habit and tentatively correlated microaporan- Denholm, 1989a, b). This prevents objective de- Volume 79, Number 3 Bateman et al. 505 1992 Arborescent Lycopsid Phylogeny

TAELE 1. List of OTTJa (1-16) with selected synonyms and bibliographic sources. OxroaAia. sp. nov. (2a) was not used as an OTU as it did not differ from 0. gracdis (2) in the qualitative characters scored.

Num- ber Taxon 1 Paurodendron.fTaipon,tii(Le,c\f.\:c([) Fry (syn. BotryoptsrU fiaipontii, Selagineiia fiaipondi) Fry (1954); Phillips & Leisitian (1966); Schlanker & Leisraan (1969); Rothwell & Erwin (1985) 2 OxToadia gTacilis Alvin Alvin (1965, 1966); Long (1964, 1971, 1986); Bateman (1983, 1992) 2a OxroaAia. sp. nov. Bateman (1983, 1992) 3 Anabatkra. pulckerriaia Witham (syn. Paralycapoditea hreuifoUiM, Lepidodsndron. brevifoUiiiTi pro parte) Felix (1954); Brack (1970); IMorey & Morey (1977); DiMichele (1930) 4 Chalon&Tia cormosa (Newberry) Pigg & Rothwell (syn. Poiyaporia mirahUis) DiMichele et al. (1979); Pigg & Rothwell (1979, 1983a, b, 1985) 5 SigilUiria approxim/ita Fontaine & White SchopC (1941); Delevoryas (1957); Eggert (1972) 6 Sigillaria sp. nov. Brongniart (1836); Benson (1918); Lemoigne (1961) 7 Synchysidefniroti sp. npv. DiMichele (1979b, 1981); DiMichele & Bateman (1992) 8 Syachyiidendron. dicenirUum (Felix) DiMichele & Bateman (syn. Lepidod^ndjoti dicetitTicuniy Diaph^rod&nAran dicentricum) Arnold (1960); DiMichele (1979b, 1981, 1985); DiMichele & Bateman (1992) 9 Diaphorodendron phdlipill DiMichele (syn. Lepidodendron pkillipsii) DiMichele (1931, 1985) 10 Diaphorodendron vas£iilare (B'mnay) DiMichele (syn. Lepidodeadron vasculare} Carruthers (1869); Hovelacque (1892); Seward (1910); DiMichele (1981, 1985) 11 Diapkorodeadron. scleroticam (Pannell) DiMichele (syn. Lepidodeadron. .iclerotUiim) Pannell (1942); DiMichele (1981, 1985) 12 Hizemodeadron. serratum (Fe\i:x) Bateman Si DiMichele (syn. Lepidodendron s^rratum) Felix (1952); Baxter (1965); Leisman & Rivera (1974); DiMichele (1981, 1983); Bateman & Di- Michele (1991) 13 Lepidodendron. kickli Watson (ayn. L. aouleatum. pro parte, L. ohovatum pro parte) Scott (1906); Seward (1906); Watson (1907); DiMichele (1983); Willard (1989a) 14 Lepidophloios karcourtii (Witham) DiMichele (syn. Lepidodendron ha.rc.ou.rtii) Bertrand (1891); Seward (1899); Zaiessky (1912); Koopmans (1923); Calder (1934) 15 Lepidopkloioa joknsonii (Arnold) DiMichele Arnold (1940); DiMichele (1979a); Winston (1988) 16 Lepidopkloioi hattii (Evers) DiMichele Evers (1951); Felix (1952)^ Andrews & Murdy (1958); Brotzraan & Schabiliov (1972); DiMichele (1979a)

limitation of individual organisrns into species u^ing phenotypy (e.g., Bateman & Denbolm, 1989c). morphological discontinuities and hinders atternpts Ironically, this inability to resolve variation at the to distinguish genetic (and thereby taxonomically whole-organism level can be considered advanta- and pbylogenetLcaUy usefid) contributions to phe- geous in a cladistic analysis. In most cases, less notype from those caused by ontogeny and eco- information is discarded when a paleobotanical spe- 506 Annals of ttie Missouri Botanical Garden

TABLE 2. Correlations of organ-apeciea that constitute the whole-plant OTUa listed in Tahle 1. Asterisked whole- plant species lack recognised autapomorphies (see caption to Table 3 for explanation of ahhreviationa).

OTU Rhiiomorph Vegetative axsi Cones PNFR • Paurodetidrofi fraipotitii- *Selagin.ellites crasiicinctas (^) OXGR* • QxToadiCL graciUs OXNS* • Oxroadia ap. nov. ANPU Sdgmaria ficoides Anohathra palcherrima Fl&mingites divenus/ickopJU. (^) CHCO 4 SIAP Sdgm/tria sp. nov. SigiUaria approximaia Mazocarpon oediptefiiiLTtL (9-*-^) SINS* Stigma-Tut ap. nov. Sigdlaria sp. nov. Mazacarpoa schareri&e/cashii (54-6) SYNS StigmaTia ficoides Synchysidsadron. sp. nov. Achlamydocarpoa variu^ (?"^5) SYDI StigmaTia ficoides Synchysldeadron. dlc&ntriciim, Achlamjydocarpoa variu^ (^+5) DIPH Stigmaria ficoidei Diapkorodeadron pkiiUpsii Achlamydocarpon varius (2+6) DIVA* Stigniaria jicoUies DiaphorodendTon vasculare Ackiamydocarpon varius (2+6) DISC Stigmaria jicoides Diaphorodendron, iclerotUum Achiatnydocarpon vaiius (2+6) HZSE* Hizettiod^ftdroti serratuni Achlamydocarpon sp. nov. (9) Lepidostrobiis minor (6) LNHI StigitiQjLcL jicoid^s L^pidod&ndron hlckd Achlamydocarpon takhtajanii (2) Lepidastrobu^ cf. oldk^mius (6) LSHC* Stigmaria ficaides L&pidopkloioa karcaurtii Lepidacarpan. lomajci (2) Lepidostrobws oldkamius (i) LSJO* Stigmaria Jicoidss Jêpidophloios johnônii Lepidocarpon iomaxi (9) Lepidostrobiis oldkamiiM (i) LSHL Stigmaria jiôulÂ LepidophloioA hallii Lepidocarpon Iomaxi (2) Lepidostrobus aldkamias (6)

cies is reduced to a single unvarying (and thus, by Partitioning a representative, conceptual organ- definition, typological) data set (the normal pro- ism of a species into morphological characters ia cedure prior to cladistic analysis) than in compa- based on the assumption that each character rep- rable studies of extant species. Also, the paleobot- resents a discrete, recognizable, and homologous anist is effectively constrained to conceptual feature. This is the most subjective and ultimately morphospecies and is therefore spared the trauma most influential phase of any cladistic analysis; it experienced by neobotanists when selecting an ap- is especially unfortunate that the only sources of propriate species concept (cf. de Queiroz & Don- evidence to support assertions of homology are oghue, 1988, 1990; Nelson, 1989; Wheeler & circumstantial; consequently, such assertions can- Nixon, 1990; Nixon & Wheeler, 1990). Although not be conclusively verified (e.g., De Beer, 1971; we wished piitnarily to investigate generic rela- Riedl, 1979; Patterson, 1982; Kaplan, 1984; Roth, tionships, our use of species (of whatever kind) as 1984, 1988, 1991; Tomlinson et al., 1984; NefF, basic operational taxonomic units (OTUs) created 1986; Ridley, 1986; Bryant, 1989; G. P. Wagner, fewer difficulties when typologically eliminating in- 1989). Features that do not vary among the chosen tra-OTU variation than the more common ap- OTUs provide no information on their phylogenetic proach of selecting sets of OTUs from higher (and relationships, though such characters are valuable often variable) levels in the taxonomic hierarchy in characterizing the entire ingroup (they may, of (cf. Doyle & Donoghue, 1986b). course, have a greater level of universality than the ingroup alone). Continuously variable characters can be artificially partitioned into binary or SELECTTON, PARTIXRONING, AND POLARIZATION OF multiple character states (e.g., by gap coding (Ar- CHARACTERS chie, 1985) or segment coding (Chappill, 1989)), The provisional selection of whole-plant species but we believe that such "soft" characters are more preceded the partitioning of the conceptual organ- appropriately analyzed by phenetic methods (cf. isms into characters and, subsequently, of the char- Bateman, 1990a; Farris, 1990). We therefore ex- acters into putatively homologous character states. cluded continuous (metric) and quasicontinuous Our chosen characters are listed below; they are (meristic) characters from our data matrix, even identified by numbers prefixed by the letter C. though they were the only potential source of unique Volume 79, Numbers Bateman et al. 507 1992 Arborescent Lycopsid Phylogeny

TABLE 2. Continued.

Megaspo Microspore TriaiigulatUporitei trlangaiatus CirrltrircidLates unnuhitiLs Setispora subpalaeocristfUa Aaroraxpora cf. a.ipereUa 'A' S^ti&parOr pannosa Aaroraspora, cf. aipereUa 'B' Lagenicula rtigoia Lycospora oTbidild ValvUUporitei ai^ritm Endo&parit&s orn^tas Tiib&TcuhLtispoTiies reinschii Cra^sispora kosankei TiLh&rciiULtispQrites rrtamillarLiis Crassispora sp. nov. Cystosporitei variu^ Granaiporite.i medius Cystoiporitei varitis Granasporites medius Cy3to>pont£> varitis Granasporites medius Cystmporites varias Gfo-rnLspofiles medius Cysto^porkes varitii GrarnLspofites madias Cystosporite.i giganteus Lycospara cf. pasiUa

Cystosporite-i gigantei^s Lycospora pusUla.

Cystospofites giganteus LycospoTo, peiiacida

Cystoiporite> gigajiteas Lycospara sp^ ripv.

Cystosporites gigantem Lycospora granuiata

(and thereby distinguishing) characters for eight a{ perjderm (C39-C43) anatomy, occur in complex- the 17 species initially selected for study (Tahle es. In such cases, a broad concept of character 2). can be selected, allowing coding jnmultistate rather We opted for a uniformly bistate data matrix, than bistate format. Such multistate characters tend on the grounds that bistate characters are more to be especially difficult to polarize satisfactorily readdy analyzed algorithtnically and the distribu- and may have to be input unordered. If they are tions of character states on the resulting trees are to be ordered, several methods are available for more easily interpreted. This decision had three coding and polarizing such characters (e.g., O'Gra- potentially deleterious consequences: dy & Deets, 1987). The preferred options are First, the hierarchy of organs that constitute the additive binary coding (Brooks, 1984) or nonre- plants introduced a degree of character duphcation; dundant linear coding (O'Grady & Deets, 1987; we often found it necessary to include a character O'Grady et al., 1989). Both operate via a hypo- scaring an organ present or absent (e.g., the rhi- thetical tree representing transitions between the zomorph: C8) before partitioning additional char- polarized multiple states of the character in ques- acters {C9-C13) to describe its detaded morphol- tion. By reducing the character states to a set of ogy in those OTUs that possess that structure. This bistate subsets, additive binary coding labels every is to be expected, given the strongly hierarchical node of the character tree and thus generates a nature of morphological and anatomical homologies Large number of narrowly defined operational char- (Riedl, 1979; Fortey & Jefferies, 1.982; Wimsatt acters. Nonredundant Unear coding avoids this pro- & Schank, 1988; Roth, 1991). We adopted a liferation of characters, but at the expense of re- simdarly relaxed attitude to the inclusion of poten- taining characters in a multistate format and tially coupled characters "correlated for develop- arbitrarily designating within the tree a major axis • mental-genetic reasons" (Doyle & Donoghue, that forms the basis for coding the remaining 1986b: 338); indeed, we hoped that our analysis branches (minor axes). Once mixed with other (typ- would reveal such character correlations, which ically mostly bistate) characters, multistate char- are by no means intuitively obvious a priori. acters complicate the generation and subsequent Second, even more complicated hierarchies of interpretation of cladograms (e.g., Gensel, 1992). related characters, such as stelar (C14-C19) and We therefore preferred the more primitive but also 508 Annals of the Missouri Botanical Garden

more intuitive additive binary system, despite the eventuaQy accepted: 69 are vegetative (CI-C4, risk of eliminating a priori some ambiguities in the C8-C72) and 46 are reproductive (C5-C7, C73- data. C115). The large number of characters reflects Third, polarization of spore ornamentation char- the stringent selection criterion of detailed knowl- acters was rendered especially problematic. They edge that was applied to potential OTUs; inclusion tend to be evolutionarily displacive rather than of poorly known OTUs would have increased the additive; there appears to be a developmental con- proportion of missing values in some characters straint on the range of features exhibited by the sufficiently to warrant exclusion of those characters exine of any one species, so that a new type of from the data matrix. ornamentation supplants rather than supplements the previous type. We spurned the option of scoring THE CHARACTERS these characters as unordered multistate in order Characters are apportioned into 11 categories: to maintain a uniformly polarized binary matrix. the overall habit of the organism (A) and ten con- Thus, we treated each type of spore ornamentation stituent organs (B-K). For each category, lists of as a separate character and assumed a hypothetical characters and character states are preceded by plesiomorphic spore lacking aQ features. discussions of relevant homologies and descriptive Polarization also presented a more general prob- terms. lem. AQ three OTUs (Oxroadia gracUis-Oxroadia sp, nov., Paurodendron fraLpontii, Ckalonena A. Habit (7 characters) cormosa) originally screened as potential outgroups {Maddison et al., 1984) exhibited some character We perceived habit as an overall property of states that we were reluctant to regard as plesio- an organism, expressed as a specific hauplan. We morphic. In Oxroadia and Paurodendron, we ini- describe the group of habits colloquially known as tially beUeved that such characters were few and trees (Cl) as "arboreous," and use "arborescent" almost confined to spore ornamentation. However, strictly to describe the ahUity to generate secondary Chaloneria proved too derived to root the tree tissues (C29). Thus, aQ 16 OTUs are considered successfully. Consequently, we constructed a hy- arborescent, but only 12 are truly arboreous. We pothetical ancestor possessing putatively plesio- reject the frequently used term "secondary wood," morphic states for aQ characters; it largely reflected because wood is by definition secondary. Ordy ma- character states shared by Oxroadia and Pauro- ture woody plants greater than 2 m in:^veraQ height dendron, though for a few problematic characters are termed trees; Chaloneria does not quaUfy as we elected to screen more distantly related lycop- a tree on this criterion, despite possessing wood sids for presumed plesiomorphic states. {albeit poorly developed) and an elongate, un- As in aQ cladistic analyses, our recognition of branched, upright stem {Pigg & RothweU, 1983a, alternative character states as plesiomorphic and b). Recumbent OTUs generating limited amounts apomorphic preceded tree-huQding. We restrict of wood are termed pseudoherbs {Bateman, 1988, these terms to character states and use primitive 1992; DiMichele & Bateman, 1989; Bateman & and derived to describe the relative positions of DiMichele, 1991). OTUs on the resulting trees. In lepidodendraleans, the main aspects of habit Many of the characters considered for inclusion are stem length {C2), frequency of lateral and were rejected on the grounds that they were known terminal branching (C3-C4, C6), and the position for less than two-thirds of the OTUs. The most on the hauplan of reproductive structures (C5- important examples are the detaUed histology of C7). Various combinations of these character states the rhizomorph and rootlets (which are well known generate several distinct architectures (Figs. 1, 2). for the form-species Stigmaria ficoides but not for Four of these characters (C3-C4, C6-C7) reflect the different types of this rhizomorph correlated the mode and timing of branching during ontogeny. with specific whole-plant species), of the leaves Lepidodendralean stems branched isptomously {or (well-documented only for Oxroadia: Bateman, near-isotomously) only during the final stages of 1988), and of the gametophyte (described for few growth (Walton, 1935; Andrews &L Murdy, 1958; cone-species; e.g., Galtier, 1964, 1970; Brack, Eggert, 1961; Wnuk, 1985); terminal branching 1970; PhiEips, 1979; Stubblefield & RothweU, is profuse in most OTUs, but infrequent in Ana- 1981; Pigg & RothweE, 1983b), and ultrastruc- bathra, Sigillaria, and Diapkorodendron, and ab- ture of spore walls (e.g., T. Taylor, 1973; W. sent in Chaloneria (C3). Strongly anisotomous api- Taylor, 1990). cal divisions during stem growth result in lateral One hundred fifteen histate characters were branches that were deciduous (04) in aQ OTUs Volume 79, Number 3 Bateman et al. 509 1992 Arborescent Lycopsid Phylogeny

except Diaphorodendron scleroticum., where thick equivalent of a primary thickening meristem. Such bark and wood suggest retention (DiMichele, 1981). branched rhizomorphs were considered radically The anisotomies terminate in cones {C6), either different from other unbranched rootstocks, wheth- individually on short peduncles {Sigillaria.) or col- er radial, as ui Paurodendron (Rothwell & Erwin, lectively on large, repeatedly dichotomoua pedun- 1985), or bilateral, as in Protostigmaria-Lepi- cle systems {C7; Anabathra and Diaphoroden- dodendropsis {Jennings, 1975; Jennings et al., dron). In all other OTUs, anisotomous cone-bearing 1983), CfeaZoneria (Pigg & RothweU, 1983a; Pigg branches were borne only on the terminal, isoto- & Taylor, 1985), and hoetei (Karrfalt & Eggert, mausly branched, determinate crown. We regard 1977 et seq.; Karrfalt, 1984). However, other cauline peduncles and cone-bearing lateral branch- studies of rhizomorphs have rendered less profound es as homologous {DiMichele & Bateman, 1989). the distinctions between radial and bilateral sym- Chaloneria lacked cones (C5), instead bearing spo- metry (Karrfalt, 1981, 1984; G. W. Rothwell, rophyUs directly on fertile zones of the unbranched pers. comm. 1989) and branched and unbranched stem (Pigg & Rothwell, 1983a, h). Consequently, vasculature (Bateman, 1988). In our analysis, bi- it is scored as missing for C6 and C7. lateral symmetry {C9) is retained as a character Polarity decisions for several of the habit char- state; it is scored as an autapomorphy of Chalo- acters were taken with considerable reservations neria and thus does not affect tree topologies. (especially Cl, C2 and C7). Also, in retrospect, the Scaring the rhizomorph of Oxroadia as branched addition of a character representing equality of is an oversimplification; it is extremely compact, "crown" branching among the pseudoherbs would so that the cortex branches shallowly and less fre- have distinguished Oxroadia ~(AoTams.n\\y isoto- quently than the vascular system {Long, 1986; mous) from Paarodeiidron a'nd Hizemodertdron Bateman, 1988). {both dominantly anisotomous). Stigmarian axes exhibit a suite of anatomical character states that, with sufficient study, can be 1. Nonarboreous {0); arboreous (1). shown to parallel those of cori-elated stem genera. 2. Stem short (relative to any branches), plant Given the current paucity of such studies, we used recumbent (0); stem tall, plant upright (1). ordy one such character: the ovoid rootlet gaps 3. Dichotomy of trunk apex frequent {0); infre- (C13) found in Chaloneria {Pigg & Rothwell, quent or absent (1). 1983a) and Sigillaria approximata (Eggert, 4. Persistent lateral branches absent (0); present 1972). (IJ. 5. Cone present (0); cone absent (1). 8. Rhizomorph absent {0); present (1). 6. Lateral branches and/or cone peduncles borne 9. Rhizomorph symrnetry radial (0); bilateral {1). on dichotomous crown {0); excurrent trunk (1). 10. Rhizomorph branched (0); unbranched {1). 7. Number of cones on lateral branches one (0); 11. Secondary xylem in rhizomorph absent {0); more than one {1). present {1). 12. Rootlets absent (0); present (1). B. Rootitock (6 characters) 13. Rootlet gap in wood fusiform (0); ovoid (1).

Until recently, the atigmarian rhizomorph (C8) C, Stele (18 characters) was regarded as arguably the most rehable ubiquitous character state defining the Lepidodendrales The morphology and histology of lepidodendra- (e.g., Phillips & DiMichele, 1992). RothweU (1984) lean vascular systems, described in detail by pre- and Rothwell & Erwin (1985) suggested that the vious authors, are valuable for distinguishing both stigmarian rhizomorph is a shoot system modified genera and species (Fig. 4a). Unfortunately, much for rooting; we recognize that it is a shootlike de- less attention has been paid to determining ho- velopmental system, hut prefer to regard it as a mologies and polarizing these complex characters. unique organ reflecting limited developmental op- We recognize six distinct forms of stelar medul- tions within the arborescent lycopsid bauplan. The Lation (C14-C19). All genera but Diaphoroden- rhizomorph is radially symmetrical (C9), undergoes dron and Synchysidendron are regarded as prim- repeated isotomous apical dichotomy (CIO), is itively protostelic {C14). The protosteles of woody (Cll), and emits in helical rhizotaxy rigid Anabathra, Chaloneria, SLgMaria, Hizemaden- absorbent rootlets (C12), each containing a single dron, Lepidodendron, and Lepidophloios are monarch vascular strand. Rothwell & Pryor (1990, medullated{C15). The core of the stele consists of 1991) concluded that the tracheary elements of unlignified cells whose dimensions are typical of such rhizomorphs are derived largely from the tracheids, suggesting that they are procambial de- 510 Annals of the Missouri Botanical Garden

FcGtJElE 4. Morphological and anatomical terminology for arborescent lycopsids.—a. Axial anatomy (redrawn from fig. 9.44 of Gifford & Foster, V989: pc = parenchymatous core, px — protoxylem, mx — metaxylejn, ax = secondary xylem, vc = vascular cambium, ph = phloem (primary), ic = inner cortex, mc = middle cortex, oc = outer cortex, pr = periderm, pd = phelloderm, pg = phellogen, pm = phellem, It = leaf traces, Ic = leaf cushions),— h. External morphology of leaf hase following leaf loss (modified after fig. 11.3B of Stewart, 1983: Is — leaf scar, vt = vascular trace, fp ~ foliar parichrios, Ip = ligule pit, uf = upper field, uk — upper keel. If = lower field, Ik ^ lower keel, p = plications). ~c. External morphology of aporophyll (modified after fig. 11.16C of Stewart, 1983, and fig. 2A of Phillips, 1979: p = pedicel, a = alations, h = heel, Im = lamina, Ig = ligule, s = sporangium, vt = vascular trace).—d. Leaf anatomy in proximal transverse section (modified after fig. VI.9E of Stewart, 1933, and fig, lA of Reed, 1941: vt = vascular trace, ss = sclerenchymatous sheath, m = meaophyll, e = epidermis, ah = lateral ahaxial grooves, ad = median adaxial groove).~e. External morphology of spore (pp = proximal pole, dp = distal pole, ph — proximal hemisphere, dh = distal hemisphere, e — equator, ts — triradiate (trilete) suture, 1 = laesura, c = curvatura, cf = contact face).

rivativea that remained paretichymatoua (Walton, had a true pith sensu Beck et al. (1982). The two 1935; DiMichele, 1979a, b). Iti Lepidodendron Synckysidendron. species share the synapomorphy and two of the three LepidophUiios species, ran- of a solidly parenchymatous pith (C17), and each dotnly oriejited filamentous cells apparently infilled possesses a histological autapomorphy: secretory a central cavity (C16; DiMichele, 1979a). In Dia- cells in Synckysidendron sp. nov., and secondarQy phorodendron. and Synchysidejidron, central pa- thickened cells in S. dicetitricum. renchyma cells are distinctly smaller than those of Deep parenchymatous invaginations in S. di- associated tracheids, snggesting that these genera centricum. and Synckysidendron. sp. nov. (C20) Volume 79, Number 3 Bateman et al. 511 1992 Arborescent Lycopsid Phylogeny

are not considered homologous with the shallower invaginations of Ckaloneria (C21); in the Syn- ckyiidendron species, the parenchyma to us wedges are raylike, ttiany cells wide and high, and are often confluent with the pith parenchyma (Di- Michele, 1980, 1981). In contrast, the invaginations of Chaloneria are smaller and do not reach the central parenchymatous area of the stele (DiMichele et al., 1979; Pigg & Rothwell, 1983a). Protoxylem configuration and leaf trace emission comprise an integrally linked complex of characters (C22-C28; Fig. 4). Protoxylem is exarch in aQ OTUs and, with the exception of Ox.roa.dia and PaurodenAron, forms a continuous sheath enclosing the metaxylem (C22). Concentrations of protoxylem observed in transverse sections of axes of many genera are often described individually as "poles" or "points" and collectively as a "corona." This two-dimensional terminology is misleading; protoxylem actually occurs as more-or-less longi- 1 1 tudinal strands that are raised to form ridges in + : "coronate" genera (Batemati, 1988). These protoxylem strands are longitudinal and linear in I k 1 f Ox,roadia, Paurodendron, and Lepidodendron, \ 1 1 1 but reputedly anastomose in Lepidopkloios (C28; * 1 f 1 Bertrand, 1891). 1 1 i 1 We have coined new terms for four distinct modes of leaf trace emission (C23-C25; Fig. 5). Leaf traces departing from a longitudinal protoxylem ridge are termed evagtnate. Those of Oxroadia and Paurodendron are emitted from a single uninterrupted ridge and are termed evaginate-direct (Fig. 5a), Those of Lepidopkloios originate within a protoxylem ridge at the point where it bifurcates and are termed evaginate-internal * I (C25; Fig. 5d). Most of the genera lack discernable I I protoxylem ridges and are said to emit superficial I * leaf traces (C23; Fig. 5b). In Chaloneria, the trace I I originates from a submarginal position in the stele and is associated with shallow parenchymatous invaginations (C24, Fig. 5c; DiMichele et al., 1979; Pigg & Rothwell, 1983a). We used X-coding (Doyle & Donoghue, 1986b) to permit evolution of evaginate-internal and invaginate states directly from

FIGURE 5. Protoxylem morphology and modes of leaf tr5.ce emission. Transverse section above, lorigitiidinal pro- jection of surface of xylem bundle below. Protoxylem in black, spots = leaf traces, solid lines = ridges, dashed lines = leaf trace orthostiches where these do not coincide with ridgea.—a. Evaginate direct: Paurodendron and Oxroadia. — b. Superficial; Anabatkra, Hi'zem.odendron, and Lspidode.ndTon.~c. Invaginate; Chaloneria.-—d. Evaginate internal: Lepidophloioi. 512 Annals of the Missouri Botanical Garden

the plesiomorphic evagiaate-direct state (tjius by- 29. Secondary xylem in trunk absent (0); passing the superficial state), but to inhibit im- present (1). probable evolutionary routes that treat the evagi- 30. Secondary xylem in lateral branches and/ nate-internal and invaginate states as intermediate. or peduncles absent (0); present (1). The stele morphology and leaf trace emission of 31. Rays homogeneous (0); heterogeneous (1). Slgillaria are especially difficult to interpret. The undulatory outer margin of the continuous primary D. Cone.x (5 characters) xylem sheath represents tangential variation in the amount of primary xylem produced; protoxylem AU OTUs possess a three-zoned cortex (C32; thickness is greatest on the flanks of the undula- Fig. 4a). It consists of a narrow inner cylinder of tions. In contrast with other genera possessing dis- compact, barrel-shaped parenchyma cells, a thick cernable protoxylem ridges, sigiUarian leaf traces middle cylinder of even thinner-walled, more-or- appear to originate from the intervening troughs, less isodiametric parenchyma cells that often decay leading to suggestions that each trace may he de- to leave a cavity, and a broader outer zone of rived from both of the adjacent protoxylem ridges thicker walled ceQs that are longitudinally elongate (e.g., Lemoigne, 1961), However, we were unable (especially in the central portion of the cylinder of to confirm their putative bipolar origin and there- tissue) and often grade into sclerenchyma (partic- fore scored SigUlaria leaf traces as superficial. ularly in the smallest diameter ceQs, close to the The alternative option of recognizing SigUlaria epidermis). This peripheral sclerenchyma is es- traces as bipolar would generate an additional ge- pecially weU developed in Diapkorodendron scte- nus-level autapomorphy. roticum.. Leaf traces passing through the middle Secondary xylem occurs in.tbe stem and at least cortex are ensheathed with cells characteristic of, the more proximal crown branches (if present) of and in continuity with, the inner cortex; they are aUOTUs(C29), but extends into the lateral branch- secretory in several OTUs (C33) and adaxiaUy es (C30) only in Diaphorodendron vasculare and concentrated in Synckysiderhdron. sp. nov. (C34). D. scleroticiun. Most OTUs possess homogeneous In Sigillaria&p. nov., Synchysidendron, and Dia- rays composed of small-diameter cells, though het- phorodendron, each leaf trace is surrounded by a eroceUular rays characterize Synchysidendron. broad cylinder of thinner-walled cells when passing Consistent nonpreservation prevented character- through the outer cortex (C35), increasing appar- ization of the phloem. ent ceQular heterogeneity. No attempt was made to divide variations in the angle of passage of the 14-19. Solid protostele (000000); medullated leaf traces through the cortex into discrete char- protostele (010000); medullated proto- acter states. Vertically elongate cavities at the cor- stele with filamentous core (011000); si- tex-periderm transition (C36) characterize D. phil- phonostele with mixed pith (100000); si- lipiii. phonostele with solidly parenchymous pith 32. Outer cortex two-zoned (0); three-zoned (1). including secretory cells (100110); si- 33. Intracortical leaf-trace sheaths not secretory phonostele with solidly parenchymous pith (0); secretory (1). including cells with secondary waQ thick- 34. Intracortical leaf-trace sheaths circumferen- enings (100101). tial (0); adaxial(l). 20. Deep parenchymatous invaginations or 35. Thin-walled parenchyma surrounding leaf trace radial partings absent (0); present (1). in thick-walled outer cortex absent (0); present 21. Shallow parenchymatous invaginations (1). absent (0); present (1). 36. Cavities at outer cortex-periderm transition 22. Exarch protoxylem sheath discontinuous absent (0); present (1), (0); continuous (1). 23-25. Leaf trace origin evaginate, direct (000); E. Periderm (14 characters) superficial (100); invaginate (XIO); evaginate, internal (XOl). Periderm occurs in all of the OTUs (C37), though 26. Longitudinal ridges of protoxylem strands its distribution (and thereby its protective and sup- discernable (0); indiscernable (1). portive function) is extremely restricted in the bau- 27. Leaf trace originates from one protoxylem plans of Oxroadia and Paurodendron. Common strand (0); two protoxylem strands (1). references to periderm as "secondary cortex" are 28. Anastomoses of protoxylem strands ab- an anatomical non sequitur; cortex is a region of sent (0); present (1). an axis (between the stele and the epidermis) rather Volume 79, Number 3 Bateman et al. 513 1992 Arborescent Ly cops id Phylogeny

than a specific tissue type. The periderm of most mechanisms (C44-C46). The first two are, by def- genera cannot be dLfferejitjated histologically into inition, mutually exclusive; interareas exhibit either phellem and phelloderm. The exceptions are Dia- a plastic response and expand (C44; SigillarUt and pkorodendron, and Synckysidendron, where clear Synckysidendron) or a brittle response and fissure bizonation ia strong evidence for a bifacial cambial (C45; Diapkorodendron) (DiMichele, 1981). In layer that produced much greater quantities of contrast, Lepidodendron hickii accommodates centripetal phelloderm than centrifugal phellem growth by expansion of cells beneath the cushion (C38; DiMichele, 1981). Additional, indirect evi- (C46; DiMichele, 1983). This character state could dence indicates bifaciality in Anabathra (Di- have replaced interarea expansions or fissuring, or Michele, 1980) and Lepidopkloios (DiMichele, it could have arisen directly from the plesiomorphic 1979a). Given the determinate growth and early state; it is X-coded to allow any of these options. onset of peridermal cambial function that are ev- Evidence for the interarea expansion of Lepido- ident in lepidodendraleans, the catnbial layer may dendron is confined to compression fossils (Tho- have fully differentiated or been active only near mas, 1966). the apices of stems and rhizomorph axes. Either 37. Periderm in stems absent (0)j present (1). phenomenon would inhibit preservation of the cam- 38. Phellem and phelloderm not histologically bial layer per se. It is also possible that the cen- differentiable (0); histologically differen- tripetal and centrifugal products of cell division are tiate (1). sufficiently similar to prevent recognition of a po- 39-43, Cellular composition of periderm uniform tentiaQy fully differentiated cambium. (00000); cells form two or three distinct Periderm is the most abutidant tissue type pro- zones (1X000); bands of resinous cell clus- duced by arboreous lycopsidis and often occurs as ters (01000); periderm bifacial, alternat- abundant disarticulated fragments in coal-baU as- ing bands of thick- and thin-waQed cells semblages (PhUlips & DiMichele, 1981; DiMichele in phelloderm (00110); periderm bifacial, et al,, 1986), Fortunately, the detailed anatomy phelloderm ± uniform (00101). and histology of the periderm (C39-C43) aUow 44-46. Leaf cushion retention mechanism absent identification of five groups of OTUs. Primitive (000); tangential interarea expansion genera (Oxroadia, Pau-rodendron, Andbathra, (100); interarea fissuring (010); subcush- Chaloneria) have a uniform periderm, which is ion cellular expansion (XXI). modified to include bands of resinous cells in Sig- 47. Periderm nonglandular (0); glandular (1), illaria (C40). Diaphorodendron. and Synckysi- 48. Periderm nonresinous (0); at least par- dendron possess bifacial periderm (C41); tially resinous (1). Synckysidendron is distinguished from Diapho- 49. Leaf traces in periderm obscure (0); prom- rodendronhy its uniform (C43) rather than banded inent (1). (C42) phelloderm. Lepidodendron and Lepido- 50. Infrafoliar parichnos strands in periderm pkloios have two- or three-zoned periderm (C39) absent (0); present (1). and are X-coded for resinous cell clusters to suppress improbable evolutionary routes that attain F. Leaf bases (15 characters) histological modifications via the acquisition of zo- nation. Lepidodendralean leaf base characters are well Glandular periderm histology (C47) is shared hy reviewed hy DiMichele (1979a, b, 1981, 1983) Lepidodendron and two of the three Lepidopkloi- for anatomically preserved species and by Thomas OS species, and resinous sacs (C48) occur in Sig- (1970b, 1977, 1978) and Thomas & Meyen(1984) illaria, Lepidodendron, and Lepidopkloioi. The for adpressed species. passage of leaf traces and infrafoliar parichnos Lycopsid leaves attenuate bilaterally close to the strands through the periderm also distinguish OTUs. stem, where they are consequently most readily Prominent leaf traces, more-or-less perpendicular detached; The area proximal to the constriction to the length of the axis and surrounded by thin- persists as a symmetrical structure raised above waQed parenchyma (C49), are an autapomorphy the surface of the axis and is termed a leaf base; of Anabathra. Similarly, well-developed infrafoliar aggregates of leaf bases preserve the phyllotaxy of parichnos strands (C50) characterize Sigiltaria the axis after leaf loss. In our more primitive OTUa periderm. (Oxroadia, Paurodendron, Anabathra, Chaio- Many lepidodendraleans retained leaf cushions neria\ leaf bases are small, ellipsoid in transverse on the stem surface as periderm production ex- section, widely spaced on the axial surface, and panded axial girth. We recognize three retention are fully transitional into the leaf lamina (C51). In 514 Annals of the Missouri Botanical Garden

the more derived OTUs, the leaf base is more cushions (C52-C53). Since the early nineteenth elaborate and only a portion emits tbe leaf; it is century, the plesiomorphic condition of greater leaf then termed a leaf cushion (Fig. 4b). Such cushions cushion length than width has been crucial for typically exhibit a simple angular outline in tan- delimiting Lepidodendron sens. lat. (DiMichele, gential section: hexagonal in Sigillaria, and dia- 1983), Despite early knowledge that awarding pri- mond-shaped in Dlapkorodendron, Synchysiden- macy to this character resulted in the lumping of dron, Hizem.oden.dron., Lepi.doden.dron, and morphologically and anatomically dissimilar species LepidopMoios (this character was not coded). (e.g., Scott, 1908; Seward, 1910), only recently Cushions are further elaborated by the develop- has Lepidodendron sens. lat. been disaggregated ment of raised upper (C54) and lower (C55) keels, into the morphologically distinct segregates Ana- and by division into upper and lower fields that are 6a(/ira (DiMichele, 1980), Diapkorodendron. sens. usually separated by a lateral line (C58) and are str. (DiMichele, 1983), Synckysldendron (Di- independently plicate (C56-C57). Sigillariais ple- Michele & Bateman, 1992), Hizemodendron siomorphic for all five characters, while Diapko- (Bateman & DiMichele, 1991), Lepidodendron rodendron and Synchysidendron are apomorphic sens, str., and Lepidophloios (DiMichele, 1979a, for all five, Lepidophloios only possesses keels. 1983). Horizontally (i.e., tangentiaUy) elongate leaf Hizemodendron. possesses plications but lacks an cushions are, however, a valid generic autapo- upper keel, while Lepidodendron lacks upper field morphy of Lepidophloios, together with radial plications but possesses a lateral line. elongation (C64-C65). Obscure evolutionary re- The leaf cushion can he regarded as an elabo- lationships of the arched and the perpendicular rated leaf base and thus as fundamentally foliar states of radial elongation among different Lepi- and appendicular in nature. This interpretation is dophloios species necessitaited X-coding. supported by the leaflike structural and positional AU OTUs possess ligules (C59), and most recess attributes of leaf cushions; rejection of the foliar the ligule in the cavity that communicates with the nature of leaf cushions would require their rec- adaxial surface of the leaf base via a deep pit (C60). ognition as develop mentally distinct organs of a The plesiomorphic exceptions are Paurodendron, kind unknown in other plants. Even the relatively where the ligule is fully exposed (Phillips & Leia- simple cushions of Sigillaria are helically ar- man, 1966), and Anabathra, where it is afforded ranged, closely packed hut discrete, well-defined some protection by the leaf cushions (DiMichele, features. Leaf bases of aU the arborescent lycopsids 1980). Foliar parichnos (C61) OCCUF in aU OTUs analyzed bear ligules, which are ancestrally foliar but Oxroadia and Paurodendron (Bateman (1988) in the class (Bonamo et al, 1988). AQ of these was unable to substantiate Long's (1986) tentative characters are features of appendicular organs pro- identification of parichnos in Oxroadia). In con- duced laterally to the apical meristem through the trast, infra foliar parichnos (C62) are confined to formation of primordia. In order to he axial rather Lepidodendron

Leaf cushions, where a sharp structural (and, pre- The presence of two vascular strands (C67) is aumably, physiological) boundary is represented as autapomorphic for Sigillaria, which also shares a leaf scar. The scar is situated within the leaf V-shaped strands (C68) with Chaloneria. Dorsi- rather than at the leaf-axis junction. Deciduous ventraQy flattened strands (C69) occur in Lepl- lateral branches may abo have been shed by this dodendron, Lepidopkloios, and Diapkoroden- mechanism; according to Jonker (1976), triangular dron scleroticujn; ambiguous evolutionary pathways marks below ulodendroid scars indicate that the from plesiomorphic terete strands necessitated branches were torn away at their junctions with X-coding. All OTUs whose leaves possess nonterete the stem. However, R. A. Gaataldo (pers. comm. strands also possess pronounced lateral abaxial 1990) argued that most specimens lack these fea- grooves (furrows) containing stomata (C70; Fig. tures, which may be taphonomic overprints. 4d); these are supplemented with a median adaxial groove in Sigillaria (C71). The vascular strands 51. Leaf is outgrowth of entire leaf base (0); of most of the more apomorphic OTUs are sur- portion of leaf base (1). rounded by a sclerenchymatous sheath (G72), 52. Length: width ratio of cushions on stems though this is absent from Hizemodendron. and large branches >1; I (0); <1 : 1 (1). Angle of leaf attachment (C66) refers only to 53. Length: width ratio of cushions on small the angle subtended by the basal portion of the branches and twigs > 1 : 1 (0); <1:1(1). mature lamina relative to the distal portion of the 54. Upper keel absent (0); present (1). axis, thus avoiding the effect of recurvation in 55. Lower keel absent (0); present (I). OTUs such as Oxroadia. This character distin- 56. Upper held nonplicate (0); plicate (1). guishes genera with hispid, generally short leaves 57. Lower field nonplicate (0); plicate (1). {Paarodendron, Anabathra, Chaloneria, LepL- 58. Lateral line separating upper and lower dodendron), hut can result from one of several fields absent (0); present (I). developmental mechanisms and is therefore prone 59-60. Ligule absent (00); superficial or in shal- to homoplasy. low depression (10); in deep cavity with narrow neck (11). 66. Angle of leaf attachment relative to axial 61. Fohar parichnos absent (0); present (1). apex ± horizontal (0); acute (I). 62. Infrafoliar parichnos absent (0); present 67. Number of vascular strands per leaf one (1). (O);two(l). 63. Consistent basal limit to leaf atrophy ab- 68-69. Transverse section of vascular strand te- sent (0); present (1). rete (00); dorsiventrally flattened (IX); 64-65. Leaf cushion not radially elongate (00); V-shaped (XI). elongate, strongly arched (IX); elongate, 70. Lateral abaxial grooves absent (0); present ± perpendicular to axis (XI). at least near base (1). 71. Median adaxial groove absent (0); present G. Leaves (7 characters) at least near base (1). 72. Sheath of sclerenchyma around trace ab- Leaves are the organs most frequently neglected sent (0); present (I). when attempts are made to reconstruct lepidodendraleans. Admittedly, their deciduousness and con- H. Cones (4 characters) sequent absence from the upper axes hinders organ correlation by organic connection, but even more Intensive study of lepidodendralean reproduc- consistent disarticulation has not prevented indirect tive structures has generated thorough reviews of correlation of cone species with the vegetative axes both anatomically preserved (Arber, 1914; Bal- that bore them. Failure to correlate leaves with bach, 1967; Brack, 1970; Hanes, 1975; Phillips, their parent plants is unfortunate, as Graham (1935) 1979; Brack-Hanes & Thomas, 1983; WiUard, and Reed (1941) demonstrated the wide range of 1989a) and adpressed (Lesquereux, 1880; Kid- potentially phylogenetically valuable characters ston, 1923-1925; Willard, 1989b) organ-species. present in isolated lepidodendralean leaves, and Reproductive characters played important roles in, Bateman (1988) recorded many characters (in- the delimitation of the genera; not surprisingly, cluding details of the cuticle, epidermis, and sto- many are genus-level autapomorphies. Moreover, mata) of leaves attached to Oxroadia axes. We many of the traits are functionally linked and can discarded most of these characters for this analysis, be used to deftne reproductive strategies in the because they would have contained unacceptably same maruier that vegetative morphology defines large proportions of missing values. growth habits. 516 Annals of the Missouri Botanical Garden

All of the lycopsids included in this analysis are Comparing sporophyUs with sterQe microphyUs, heteroaporoua (C75). Oxroadia, Paurodetidron., we believe that the pedicel is homologous with the and Anabathra. have primitively bisporangiate leaf base (including the leaf cushion), and the spo- strobili (C76), with microsporangia concentrated rophyll distal lamina is homologous with the leaf toward the cone apex. The fertile zones of Ckal- lamina. We suggest that the qualifier "distal" should oneria (arguably a derived condition) are similarly be abandoned for the sporophyll lamina (there is bisporangiate; all other OTUs bore monoaporan- no proximal lamina), and that the lateral exten- giate cones. sions of the pedicel should be termed alations, ir- Characters 73 and 74 describe the relationships respective of size and orientations (use of the term to the parent stem of the lateral cone-bearing axes, "integuments" for extensive enrolled alations mis- whether peduncles or branches {Chaloneria ia un- leadingly implies homology with the integuments branched and was scored as missing for C73). of true seeds). Lateral branches are subtended by stelar gaps (C73) Little attention is paid in the literature to angle in Diaphorodendron., Synchysidendron., Lepi- of pedicel attachment relative to the cone axis dodendron, and Lepidopkhios, and are medul- (C77), which may be prone to ontogenetic change lated (G74) in SigUlaria, Diaphorodendron, Lep- as an aid to passive spore dispersal (Bateman, 1988). Ldodendron, and Lepidophloios. Thus, our identification of Oxroadia as autapomorphic for obtuse sporangia is tentative. With 73. Stelar vascular gap associated with departure this exception, all sporophyll and sporangium char- of peduncle or lateral branch absent (0); pres- acters (C78-C91) are scored as plesiomorphic for ent (I). the four most primitive OTUs possessing bisporan- 74. Pith in trace of peduncle or lateral branch giate cones {Oxroadia, Pau.roden.dron, Anabatk- absent (0); present (1). ra, Chaloneria), which differ quantitatively rather 75. Plants homosporous (0); heterosporous (1). than qualitatively. A good example is the number 76. Cones/fertile zones bisporangiate (0); mono- of megaspores per megasporangium, which also sporangia te (I). separates species of the same genus (e.g.. Ana- bathra: Felix, 1954; Brack, 1970; see also Ap- /. Sporophylls and sporangia (15 characters) pendix IB). It is tempting to distinguish qualita- Literature review suggests that the terms de- tively between megasporangia containing four scribing most components of the sporangium-spo- spores, derived from one spore mother cell, and rophyll complex have become standardized (Fig. those containing more than four spores, derived 4c). The sporophyll is divided into a proximal por- from more than one spore mother cell. However, ti.on ("pedicel"), perpendicular to the cone axis, each condition characterizes one of the two species and a distal" portion ("distal lamina"), parallel to of Oxroadia (Bateman, 1988), and spore counts the cone axis and oriented toward the cone apex. are complicated by frequent and apparently ran- The adaxial surface of the pedicel bears the spo- dom abortions. rangium and (immediately distal to the sporangium) Differences among the remaining (monosporan- the ligule. The pedicel is triangular in median trans- giate) genera focus on megas parang iate cones and verse section and attenuates abaxiaUy, to a struc- reflect their shared transition in the nature of the ture that has been termed a keel if sufficiently dispersal unit from isolated megaspores to a meg- prominent (PbiUips, 1979), and laterally, to struc- asporangium-sporophyll complex (C81). The apo- tures that have received various names. "Lateral morphic state of this character encapsulates a broad laminae" is used most commonly; alternatives are spectrum of morphologies (elaborated in C80 and "lateral extensions" (e.g., Meyen, 1987), "wirigs" C82-C90) that may reflect parallel (i.e., homo- (e.g., Arber, 1914), "flanges" (e.g., Sporne, 1975), plastic) responses to simdar selective regimes. In •and "alations" (e.g., Phillips, 1979). Some authors all monospo rang iate genera but SigdUtria, this (e.g., Phillips, 1979) have distinguished the most evolutionary trend results in reduction to a single developed state of this character (long and enrolled) functional megaspore (C90) that germinates within as "integuments," by analogy with the true seeds the sporangium (C80; Phillips, 1979). Probably as of "spermatophytes." The apically directed distal an aid to dispersal and/or protection, these changes lamina is much less three-dimensional and usually are accompanied by lateral expansion of the pedicel appears as a shallow "V in transverse section. to form alations (C82-C84). These are coded as An antapicaUy directed extension from the right- short and horizontal in SigUlaria, Diaphoroden- angled junction of the pedicel and distal lamina is dron, and Synchysidendron., short and erect in termed the heel. Hizemodendron.and Lepidodendron, &nd[ong and Volume 79, Number 3 Bateman et al 517 1992 Arborescent Lycopsid Phylogeny

erect (typically enrolled) in Lepidophloios. These (000); distally (100); proximally (010); characterizations require further revision; the lat- indehiscent fragmentation (XXI). eral margins of the pedicel can be proportioijately 90. Functional megaspores per megasporan- longer in Anahathra (e.g., fig. 9 of Brack, 1970) gium more than one (0); one (1). and more erect in Diaphorodendron and Syit- 91. Parenchyma enclosing megaspores absent chysidendron (e.g., pi. 8.4 of Phillips, 1979) than (0); present (I). those of Lepidoden-dron (e.g., pi. 5.4 of Phillips, 1979). Moreover, shortness may not he homolo- /. Megaspores (10 characters) gous between vertical and horizontal alations; bence, X-coding was used to allow evolution of short, erect Figure 4e summarizes terms describing the "ge- alations from either absence of alations or short, ography" of the exteriors of lycopsid spores. horizontal alations, and to suppress evolution of Morphological and ultrastructural studies of ly- short, horizontal alations from short, vertical ala- copsid megaspores preserved in situ in cones have tions. been undertaken since the earliest applications of palynology to bios tratig rap hie and paleoecological Megasporangia of Diaphorodeadron and Syn- problems (Schopf, 1938; Bochenski, 1939; Brack, ckysidendron are strongly dorsiventrally flattened 1970; Taylor, 1990; see also Bartram, 1987). (C85-C86) and dehisce proxitnally (C87-C89), Polarity decisions for laesural (G94-G96) and while those of HLzemodendron, LepiAadenAron,, equatorial (C92-C93) characters were problem- and Lepidophloios are strongly bilaterally flat- atic; they are generally poorly developed in dis- tened and dehisce distaUy, SigtHaria approximata tantly related lycopsids, but better developed and undergoes indehiscent fragihentation (C89), pre- more complex in putatively more closely related sumably an apomorphic character state. We have outgroups (e.g., Selaginella: Stanier, 1965; Tryon used X-coding to allow its evolution by one step & Lugardon, 1978; Minaki, 1984) and in the more from any of the three dehiscence mechanisms. primitive ingroup members {OxroadLa, Paaroden- Sigillaria approximata possesses another autapo- dron, Chaloneria) than in the more derived OTUs. morphy, the enclosure of megaspores with paren- Prominent laesural expansions characterize chyma (C9l). Oxroadia,, where they are fimbriate and do not HeteroceUular sporangium walls (C79) charac- extend beyond the curvaturae (C95; Alvin, 1965, terize Diaphorodendron and Synckysidendron. 1966; Bateman, 1988), and PauT'sden.dran., where Only Lepidodendron possesses a multiseriate spo- they are plicate and extend to the equatorial flange rangium wall; together with greater sporangium (C96: Guennel, 1952). The laesurae of Diapho- size (a quantitative character and therefore not rodendron and Sync'hysidendron. megaspores are coded), this distinguishes Lepidodendron sporan- gulate (C94); the spongy, trilobate proximal massa gium-sporophy 11 complexes from the otherwise is a key taxonomic character. Equatorial expan- identical equivalents of Hisemodendron. sions provide autapomorphies for Paurodendron, in the form of a perisporial plicate flange (C93: 77. Angle of sporophyU attachment relative Guennel, 1952), and Chaloneria, in the form of to cone apex ± horizontal (0); obtuse (1). auriculae (ear-shaped expansioixs of the exitie) op- 78. Sporangium wall uniseriate (0); multise- posite laesural rays (C92: Pigg & RothweU, 1983b). riate (1). Most OTUs lack dispersed proximal and distal 79. Sporangium, wall homocellular (0); het- ornamentation. Contact-face ornamentation is con- erocellular (1). fined to Oxroadia (sparse, robust, buttressed spines: 80. Megaspores shed from sporangium prior C97), Pa.aroden.dron (reticulate; C98), and Chal- to germination (0); megaspores germinate oneria (rugose: C99). The megaspore of Sigillaria within sporangium (1). sp. nov. could not be scored for this character, but 81. Dispersal unit megaspore (0); megaspo- its distal surface clearly bears short spines (ClOO: rangium-sporophyll complex (I). Benson, 1918; Pigg, 1983). Large and more com- 82-84. Alations of megasporophyll pedicel absent plex buttressed spines typify Oxroadia mega- (000); short, horizontal (100); short, suh- spores. Paurodendron megaspores bear a striking erect (XIO); long, erect (Oil). distal reticulum (ClOl). 85-86. Transverse section of megasporangium ± circular (00); strongly bilaterally flattened 92-93. Equatorial ornamentation absent (00); (10); strongly dorsiventrally flattened (01). auriculate (10); flanged (01). 87-89. Megasporangium dehisces longitudinally 94-96. Laesural ornamentation absent (000); 518 Annals of the Missouri Botanical Garden

gulate (100); fimbriate (OIX); plicate Leisman, 1969; Bateman, 1988). Several OTUs (0X1). lack contact-face ornamentation, but only Ckalo- 97-99. Contact-face ornamentation absent neria and Lepidophloios harcou.rtii lack distal (000); echinate (100); reticulate (010); ornamentation. In Oxroadia and Paurodendron, rugose (001). the echinate contact faces are paralleled by the 100-101. Distal ornamentation absent (00); echi- distal ornamentation (Cl 15). Diaphorodendron a.nd nate (10); reticulate (01). Synckysidendron microspores are papillate (C114), those of Sigillaria are characterized by a mixture of spines and cones (C113), and those of Hise- K. Microspores (14 characters) modendron, Lepidodendron, and Lepidopkloios Several lycopsid microspores commonly en- hallii bear dense grana (Cl 12). countered in dispersed miospore assemblages (sen- suChaloner, 1970) have beencorrelated with source 102. Pseudosaccus absent (0); present (1). cones, both anatomically preserved (Brack, 1970; 103-104. Equatorial expansion absent (00); Courvoisier & PhiUips, 1975; WiUard, 1989a) and unornamented bizonate cingulum com- compressed (Thomas, 1970a, 1987; Willard, plex (10); distally ornamented cingu- 1989b). Classification of lycopsid microspores has lum complex (01). focused on equatorial elaboration and general sur- 105. Laesurae subdued (0); strongly raised face ornamentation, Tbe only exception in our list (1). of characters, strongly raised laesurae (C105), oc- 106-108. Equatorial ornamentation absent (000); curs in ChalotiAria and LepldophloioA harcourtLL cingulum complex (100); crassitude In Ckaloneria, separation- of the sexine and (010); zona (001). nexine layers distal to the contact faces bas gen- 109-111. Contact-face ornamentation absent erated a pseudosaccus (C102: Brack & Taylor, (000); granulate (100); granulo-foveo- 1972). AU of the monosporangiate-coned genera late (010); echinate (001). exhibit some form of equatorial elaboration (C106- 112-115. Distal ornamentation absent (0000); C108). An.ahatk.ra, Hizemodendron, Lepidoden.- densely granulate (1000); echino-co- dron., and LepidophLoios microspores possess a nate (0100); papillate (0010); echinate thickened equatorial band (citvgulum: C106); in (0001). Hizemadendron, Lepidodendron., and some Lep- idophloios species, tbis is supplemented with an THE DATA MATRIX external membranous flange (zona: C108). Sigil- laria, Diaphorodendron, and Synchysidendron After alt 115 characters had been scored, two microspores bear a crassitude equatorial thickening whole-plant species (Oxroadia, gracilis and (C107) that appears structurally distinct from a Oxroadia sp. nov.) possessed identical data sets, cingulum. Cingula of some OTUs are further elab- demonstrating that they differ in quantitative but orated; those of Hizemodendron, Lepidodendron, not qualitative characters. The duplicate data set and Lepidophloios k.arcou.rtii are bizonate (C103) provided no useful information and was therefore and those of Anabathra are distally ornamented omitted, reducing tbe original 17 whole-plant spe- (C104). cies to 16 OTUs that, in our opinion, represent Characterization of microspore general surface 10 genera. Tbis gave a ratio of characters :OTUs morphology is increasingly dependent on the great- of 115:16(7.2:1). er resolution of scanning electron microscope (SEM) Tbe resulting 1,840-byte data matrix (Table 3, studies relative to light microscopy (LM). As in the excluding HYAN) contained 94 missing values that megaspores, ornamentation is described separately each reflected one of four factors. Two of these for contact faces (C109-C111) and the distal hemi- factors result from ignorance of whether the OTU sphere (C112-C115), though Lepidophloios john- possesses the feature or what state the feature sonii is insufficiently known to be scored. Contact exhibits, one from unwillingness to specify the pre- faces of Hizemadendron,, Lepidodendron, and cursor state of the character (the X-coding pro- Lepidophloios microspores are granulate (C109; cedure discussed in detail by Doyle & Donoghue, Leisman & Rivers, 1974; Willard, 1989a), those 1986b: 344-350; see also Appendix 2), and one of Diaphorodendron and Synchysidendron grade from absence of the relevant feature, which there- into a more foveolate texture (CllO; Courvoisier fore cannot be scored. The first three categories & PhiUips, 1975), and those of OxroaAia and indicate varying degrees of ignorance concerning Pau.rodendron are echinate (Gill; Schlanker & the nature of the character and can be replaced Volume 79, Number 3 Bateman et al. 519 1992 Arborescent Lycopsid Phylogeny

by a posteriori optimization, substituting values most increasing length and decreasing perceived leveb parsimonious with the cladogram in question. The of homoplasy by including characters that are, by fourth type of miasiug value (coded # in Table 3) definition, nonhQmQplastic(e.g., Brooks etal., 1986; is also replaced during optimizatioii, but here the Kluge, 1989; Sanderson & Donoghue, 1989). result is merely an operational necessity. It does 2. The apomorphic state is ubiquitous among not generate a potentially biologically mearungful the OTUs (including the outgroups If used), thereby hypothesis; there is no obvious meaning in scoring justifying their status as a potential clade. Although a character state as present for an OTU that com- such character states are conventionally described pletely lacks the feature in question (for example, as "basal synapomorphies" or "invariant charac- in Fig. 6 Ckaloneria is optimized as possessing ters" (e.g., Sanderson & Donoghue, 1989), we peduncle/branch gaps (C73) but actually lacks both prefer to coin the more parsimonious term "holapo- types of organ). This situation is more frequent in morphy." It could be argued that such character data matrices that include OTUs of highly diver- states are merely plesiomorphies, but they cannot gent morphology, where the probability of obtain- be defined as such in the absence of an equivalent ing fully compatible sets of homologous features is apomorphic state. Our definition of the term syn- less. The most gap-ridden (12% missing values) of apomorpby is also unconventional in implicitly ex- our data sets is Chaloneria. carmasa, where 11 of cluding holapomorphic character states. Holapo- the 14 missing values reflect lack of the coded morphy, like autapomorphy, is a relative concept; feature (i.e., absence rather than ignorance). Com- addition to the suite of taxa analyzied of an OTU pared with OTU selection, we were less rigorous lacking the apomorphic character state transforms when excluding gap-ridden characters from the a formerly ubiquitous holapomorphy Into a non- matrix; the worst examples (C34, C40, C69) pos- ubiquitous synapomorphy. Holapomorphies also re- sess 31% missing values, most of these X-coded semble autapomorphies in being phylogeneticaUy to represent ambiguity of precursor states. Nev- uninformative within the confines of a particular ertheless, the overall proportion of missing values data matrix. Hence, like autapomorphies, holapo- in our data matrix (5%) compares favorably with morphies should be (and in this study were) omitted those of other studies (e.g., 24% in Table 2 of from tree length calculations. Doyle & Donoghue, 1986b). 3. When the apomorphic state occurs in more We believe that every cladistic data matrix should than one but less than aU of the OTUs, it is deemed routinely carry character: OTU ratios to indicate phylogeneticaUy informative and included in the the average strength of empirical support for nodes algorithmic computation of tree length. Most such and percentage missing values to indicate the com- character states are synapomorphlc, although cat- pleteness of the data matrix, just as the resulting egory (3) also encompasses homoplasies (these are trees now routinely carry consistency indices to generally regarded as refuting the initial hypothesis summarize levels of homoplasy (Kluge & Farris, of homology between the plesiomorphic and apo- 1969; Brooks et al., 1986). morphic states: e.g., WQey, 1981; Funk & Brooks, 1990). The perception of synapomorphies as homoplastic (i.e., as parallelisms and/or reversals) or OPTIMIZATION, CHARACTER STATES, AND nonhomoplastic (evolving only once and persisting MISSING VALUES throughout the derived portion of the clade) is the The distribution of an apomorphic character least stable aspect of cladistic analysis, since these state among aU the OTUs can be assigned to one conditions are a property only of the interaction of three categories; of a specific tree topology with a specific optimi- 1. The apomorphic state is confined to a single zation algorithm (see below). Also, character states OTU and is thus an autapomorphy at the least can be both homoplastic and partially synapo- inclusive (species) level in the taxonomic hierarchy. morphic; for example, a particular state may be a It is important to note that the autapomorphic meaningful synapomorphy of the OTUs forming condition is a relative concept; a synapomorpby clade A-t-B but be represented as a paraUehsm in (shared derived character) at the species level in their non-sister OTU D (J. I. Davis, pers. comm.' our analysis can be an autapomorphy (unshared 1990). Surprisingly, the terminologicaUy rich dis- derived character) at the more inclusive level of cipline of cladistics does not appear to have gen- genus. Autapomorphies at the least inclusive level erated unique terms to describe the important (al- analyzed distinguish OTUs, but are phylogeneti- beit ad hoc) distinction between synapomorphies calty uninformative. Consequently, they are omit- sens. str. (i.e., holapomorphies excluded) that are ted from algorithmic analysis to avoid artificially homoplastic and those that are not; only the latter 520 Annals of the Missouri Botanicai Garden

TABLE 3, Cladistic data matrix. Operational taxomomic units: Hypothetical ancestor (HYAN), Paurodendron. fra.lpan.tLl (PNFR), Ox.roadia gracdis-sp. nov. (OXGR), Anahathra {Paralycopodites) pidcherHma (ANPU), Chal- otieTia. cornosa (CHCO), SLgillana approximata (SIAP), Sigillana. sp. nov. (SINS), Syru:hysidendron. (Diapho- rodendron) sp. nov. (SYNS), Synckysidendron. dicentrmam (SYDI), Diapkorodendron phdhpsii (DIPH), Diapko- rodendron va.s

Habit (1-7) Rootstock (8-13) OTU 5 10 + + @ + @ @ HYAN 0 0 0 0 0 0 0 0 0 0 0 0 0 PNFR 0 0 0 0 0 0 0 0 I ?,

OXGR 0 0 0 0 0 0 0 0 0 •0 ANPU 1 I 0 0 I 1 0 0 0 CHCO 0 I 0 1 #, #. I I I SIAP 1 0 0 1 0 0 0 I SINS 1 0 0 1 0 0 0 SYNS 0 0 0 0 0 0 0 0 SYDI 0 0 0 0 0 0 0 0 DIPH 1 0 0 1 I 0 0 0 DIVA I 0 0 1 1 0 0 0 DISC I 1 0 1 I 0 0 0 HZSE 0 0 0 0 0 0 0 0 0 LNHI 0 0 0 0 0 0 0 0 tSHC 0 0 0 0 0 0 0 0 LSJO 0 0 0 0 0 0 0 0 LSHL 0 0 0 0 0 0 0 0

Cortex (32-36) Periderm (37-50) OTU 35 40 ® + + @ 4 + 4 * * HYAN 0 0 0 0 0 0 0 0 0 0 0 0 PNFR 0 ?» 0 0 0 0 0 0 0 0 OXGR 0 0 0 0 0 0 0 0 0 0 ANPU 0 0 0 0 0 0 0 0 0 0 CHCO ?. 0 0 0 0 0 0 0 0 0 SIAP 1 0 0 0 0 0 1 0 0 0

SINS • L *0 0 0 0 I 0 0 0 SYNS 1 I 0 0 0 0 1 SYDI 0 0 0 0 0 0 1 DIPH 1 ?. 1 0 0 I 0 DIVA I 0 0 0 0 I 0 DISC I 0 0 0 0 1 0

HZSE 0 0 0 0 —, ~0 ^d ~0 ~a Q 0 LNHI 0 0 0 0 0 I X. 0 0 0 ^LSHC ?l ?<= 0 0 0 I X. 0 0 0 9 LSJO I •0 6 0 0 I x„ 0 0 0 LSHL I 0 0 0 0 1 X, 0 0 0

reliably characterize an entire monophyletic por- teriori procedure performed using one of a range tion of a clade. of algorithms that are designed to apply specific We are also surpri3ed at the paucity of literature logical precepts to specifying the nature (e.g., re- concerning optimization, as it proved to be a crucial versal vs. parallelism) and location of each char- aspect of our analysis. Optimization is an a pos- acter transition on a tree whose topology and length Volume 79, Number 3 Bateman et al. 521 1992 Arborescent Lycopsid Phylogeny

TABLE 3. Contmued. ( —), OTU possesses relevant feature but character state unknown (?), OTU lacks relevant feature (#), precursor state ambiguous (X; X-coded sensu Doyle & Donoghue, 1986b). Functional level of generality of derived character state in preferred most parsimonious tree: + = species level autapomorphy (character state restricted to a single OTU; these provide no information on historical relationships of species or genera), * = genus level autapomorphy (character state restricted to a single genua but occurring in more than one species; these provide no information on historical relationships of genera), @ = holapomorphy (= basal synapomorphy; these provide no information on historical relationships of species or genera).

Stele (14 -31) 15 20 25 30 * * + + * + + * * 4 @ + * 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 0 1 X, 1 0 0 0 #. 0 0 I 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 1 1 0 1 0 0 0 0 0 0 1 0 0 I 0 1 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 I 0 0 0 0 0 0 0 0 0 0 0 0 ' L 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 X, 0 1 0 0 1 0 0 0 I 0 0 0 0 0 X, 0 1 0 0 1 0 0 0 1 0 0 0 0 0 X, 0 1 0 0 1 0 0

Periderm (cont'd.) Leaf bases (51 -65) 45 50 55 60 * + + * * ® 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 #« #« #, #» # # D #, 0

0 0 0 0 0 0 0 0 #« #. #, #, # # Q #0 1

0 0 0 0 0 1 0 0 #= #= #« #. # # Q #0 0 0 0 0 0 0 0 0 0 #. #. #. #. #< # a #, I 0 0 0 1 0 1 0 1 0 0 0 0 0 I 0 0 0 1 0 I 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 X. X, 1 I I 0 0 0 1 0 1 0 0 0 1 1 0 0 1 1 0 0 0 0 0 0 1 1 0 0 I I 0 0 0 0 0 0 0 1 0 0 1 1 0 0 0

have already been fixed. In theory, optimization had the advantage of maximiaing the number of cannot alter the length of a tree (though see below optimization algorithihs that could legitimately be for a critical reappraisal of this conventional wis- applied (Swofford, 1985; 3.10). We tested aU five dom). optimization algorithms available in PAUP 2.4: Rooting the tree using the hypothetical ancestor ACCTRAN maximizes reversals, as in practice does 522 Annals of the Missouri Botanicai Garden

TABLE 3. Continued.

Leaf bases (cont'd.) Leaves (66-72) OTU 65 70 * + * * HYAN 0 0 0 0 0 0 Q 0 0 0 0 0 PNFR 0 0 0 0 0 1 0 0 0 0 0 0 OXGR 0 0 0 0 0 0 0 0 0 0 0 0 ANPU 0 0 0 0 1 0 0 0 0 0 0 CHCO 0 0 0 0 I 0 X. I 1 0 0 SIAP 0 0 0 0 I X. I 1 1 SINS 0 0 0 0 I X. I 1 I SYNS 0 0 0 0 0 0 0 0 0 SYDI 0 0 0 0 0 0 0 0 0 DIPH 0 0 0 0 0 0 0 0 0 * I DIVA 0 0 0 0 0 0 0 0 0 DISC 0 0 0 0 0 I X, 1 0 HZSE 0 0 0 I 0 0 0 0 0 LNHI I 0 0 0 0 I X, 1 0 1 0 LSHC ?, 1 X, 0 0 I X. • L

LSJO ' 1 1 X. 0 0 I X, I 0 LSHL 1 X, I 0 0 1 x> I 0

Megaspores (92-101) OTU 95 100 + + * + + + + + + HYAN 0 0 0 0 0 0 0 0 0 0 PNFR 0 1 0 X, I 0 I 0 0 I OXGR 0 0 0 I X, I 0 0 1 0 ANPU 0 0 0 0 0 0 0 I 0 0 CHCO I 0 0 0 0 0 0 0 0 0 SIAP 0 0 0 0 0 0 0 0 0 0 SINS 0 0 0 0 0 ?= ?, 1 0 SYNS 0 0 0 0 0 0 0 0 0 SYDI 0 0 0 0 0 0 0 0 0 DIPH 0 0 0 0 0 0 0 0 0 DIVA 0 0 0 0 0 0 0 0 0 DISC 0 0 0 0 0 0 0 0 0 HZSE 0 0 0 0 0 0 0 0 0 0 LNHI 0 0 0 0 0 0 0 0 0 0 LSHC 0 0 0 0 0 0 0 0 0 0 LSIO 0 0 0 0 0 0 0 0 0 0 ISHL 0 0 0 0 0 0 0 0 0 0

FARRIS; in contrast, DELTRAN maximizes par- degree, MINE. We preferred MINRES and MINF, allelisms. MINF concentrates character state tran- as they minimized perceived honioplasy in the lower sitions toward the terminal branches, MINRES (genus-level and above) branches that were of concentrates all possible transitions toward the root,- greatest interest to us; they also tended to yield then concentrates the remainder toward the ter- the greatest number of intuitively satisfactory se- minal branches. For our preferred most parsimo- lections when (1) choosing between reversals and nious tree (PMPT), FARRIS yielded similar (though parallelisms, and (2) substituting 0 or 1 for missing not identical) results to ACCTRAN, and MINRES values of specific characters (see below). Reser- yielded similar results to DELTRAN and, to a lesser vations expressed by Swofford (19S5: 3.9-3.10) Volume 79, Numbers Bateman et al. 523 1992 Arborescent Lycopsid Phylogeny

TABLE 3. Continued.

Conea (73-76) Sporophylls & Sporangia (77-91) 75 80 S5 90 + + + 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 X. Xo 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 I X. 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0

Microapores (102-115) 105 no 115 +' + 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 1 0 0 0 0 0 •0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 1 0 0 1 0 0 1 1 0 0 1 0 1 0 0 0 0 ?, 0 0 ?J ? ?. 0 0 0 0 1 1 0

concerning MINRES encouraged our consistent result are different for every tree of every analysis; use of MINF. for example, those presented as subscripts to miss- During optimization, each missing value (coded ing values in our data matrix (Tahle 3) refer only 9 in the PAUP data matrix) is replaced with 0 or to the preferred MPT of analysis A foQowuig ap- 1 in accordance with (1) the topology of the tree plication of the MINF optimization algorithm. Re- and {2) the intended effect on patterns of character placement of missing values is achieved parsimo- state transformation of the chosen optimization al- niously in accordance with the topology of the tree, gorithm (this is an a priori opportunity to modify so that further homoplasy will not be introduced. evolutionary interpretations). The substitutions that Hence, we presume that this procedure artificially 524 Annals of the Missouri Botanicai Garden

reduces levels of homoplaay relative to those that erates two topologies, A and B, both X steps in would have been determined from the same matrix length. A posteriori screening for transient autapo- if complete (i.e., gap-free). morphies/holapomorphies reveals four in topology Doyle & Donoghue (1986b; 352) imposed dual A and two in topology B. A is then preferred over origin (parallelism) where a structure was simpli- B as its true length is X — 4, relative to X — 2 fied, and an origin and a loss (reversal) where a in topology B. Unfortunately, topology C, per- structure hecame more complex, on the assumption ceived by the algorithm as X + I steps long but that "it is easier to reduce or lose a complex struc- containing six transient autapomorphies/holapo- ture than to elaborate one from a simple structure." morphies, has a true length of X — 5 steps and is We did not consider this generalization sufficiently actually the most parsimonious tree. Thus, the true reliable to warrant a posteriori modification of our lengths of trees generated from a data matrix con- algorithmically optimized character state distribu- taining missing values can only be calculated a tions, though we did emphasize complex, appar- posteriori. Algorithmically determined tree lengths ently conservative characters in subsequent evo- are unreliable, and trees other than those that are lutionary interpretations. ostensibly the most parsimonious must also be According to Bateman (in prep.), when all OTUs screened individually via apomorphy lists for spu- are scored as possessing either the plesiomorphic rious additional steps. The alternative option of or apomorphic state for a character, the assignment omitting all potential transient autapomorphies and of that character to one of these three ostensibly holapomorphies a priori (appendix 1 of Sanderson exclusively categories (autapomorphy, holapomor- & Donoghue, 1989) deleteriously discards poten- phy, synapomorphy sens, str.) \s dejw,itive\ its con- tial synapomorphies merely because their frequen- dition is fixed for that data matrix. However, this cies among the OTUs approach zero or unity. principle does not apply if the character column contains at least one missing value (9), when the PARSIMONY ANALYSIS results of optimization determine the status of the character as informative or uninforraative. For ex- Cladograms were generated from the data ma- ample, in our data matrix, a character scored as trix using Version 2.4 of PAUP (Swofford, 1985), fifteen Is and one 9 (e.g., C29) will be bolapo- which employs unrestricted parsimony via the morphic if the 9 is replaced a posteriori with a 1, Wagner method (Kluge & Farris, 1969; Farris, but synapomorphic if the 9 is replaced with a 0 1970; Felsenstein, 1982; Swoffor^, & Maddison, (in practice, this will occur only if the OTU scored 1987; Wiley et al., 1991). Some of the compu- 9 is placed at the base of the cladogram). Similarly, tational difficulties encountered by us and discussed a character scored as fourteen Os, one 1, and one below have been at least partially surmounted by 9 (e.g., C94, C98) win be autapomorphic if the 9 more recent software (see Appendix 2). Despite is replaced with a 0 but nonautapomorphic if the the long run-times incurred on our IBM-PS2/#80, 9 is replaced with a 1. Hence, there is a need for the branch-and-bound option (a modification of the the concepts of transient autapomorphy, transient algorithm devised by Hendy & Penny, 1982) was holapomorphy, and transient synapomorphy, to used routinely to obtain the definitive shortest trees. accommodate characters that contain missing val- Once character scoring had been finalized, five ues. These concepts are relative, even within a different configurations of the data matrix were single data matrix; they characterize ordy a single analyzed: combination of a specific topology and a specific A. All 16 OTUs and aU 115 characters included. optiniization algorithm. In our novel terminology, This basic analysis provided a yardstick by which definitive and transient autapomorphies together to measure the remaining analyses. constitute operational autapomorphies (likewise for B. All OTUs included, "habit" characters (Cl- holapomorphies and synaporaorphies). C7) excliided. We wished to reassess the phylogeny In contrast with definitive autapomorphies and without these characters for two reasons. First, holapomorphies, transient autapomorphies and hol^ they describe the most generalized aspects of plant apomorphies cannot be screened out of an analysis' morphology and are thus most prone to epigenesis. a priori. Consequently, they contribute to tree length Second, we wished to map the distribution of ly- as calculated during cladistic analysis; they intro- copsid bauplans onto a phylogeny constructed in- duce spurious extra steps in an unpredictable man- dependently of such characters (see also Bateman ner, often generating alternative trees that are & DiMichele, 1991; PhiUips & DiMichele, 1992). incorrectly considered of equal length by the par- C. AU characters included, but Chaloneria cor- simony algorithm. For example, a data matrix gen- mosa excluded. Survey of tree topologies from Volume 79, Number 3 Bateman et al. 525 1992 Arborescent Lycopsid Phytogeny

analyses A and B demonstrated that Chaloneria ed by the tree-buUding algorithm. Second, we wished is the most unstable OTU; Lt is supported by the to use lists of apomorphies following optimization least robust node, characterized only by homo- to assess each tree for transient holapomorphies plastic and autapomorphic characters, and pos- and autapomorphies, so that they could be sub- sesses more autapomorphies {six) than any other tracted to obtain its true length (determined entirely OTU (Fig. 6). This most awkward OTU was omitted by synapomorphjes sens. str.). In practice, this in order to determine how the topologies of the time-consuming screening procedure was not ap- more parsimonious trees would be altered and plied to trees longer than L^^.^ (a new algorithm whether homoplasy would decrease significantly. is required for this purpose), rendering optimization D. AU OTUs included, analysis restricted to veg- and the retention of apomorphy lists redundant etative characters (C1-C4, C8-C72). from L„i„+j onward (analyses A, B, D) or L^„+j E. All OTUs included, analysis restricted to re- onward (analysis C). productive characters (05-07, C73-C115). Anal- Having surveyed all optimally {L„;„) and subop- yses D and E were performed to determine the timally (L^^..^^,) parsimonious trees, we focused on relative contributions of vegetative and reproduc- particular trees of interest, including aQ most par- tive characters to the whole-plant phylogeny (cf. simonious trees (MPT, i.e., tree of length L^^J. Bateman & DiMichele, 1991), and to assess the These were reprinted with APOLIST (a list of node likely accuracy of phylogenies based on the partial by node character state transitions) and CHGLIST plants that constitute most paleobotanical "spe- (a list of character by character state transitions) cies." Data matrices for organ-species phylogenies for full interpretation (e.g., Figs. 6, 7). Topologies are much easier to construct^ than those for whole- of potential interest longer than those routinely plant phylogenies, given the'difficulty of correlating surveyed {i.e., longer than ca. L^„+j; Fig. 7) were vegetative and reproductive organs. specified using the TOPOLOGY command in "user After some experimentation, we developed an tree" mode (SwofFord, 1985: 2.20-2.22). analytical routine that was applied to each of our In summary, our cladistic analyses were exper- main groups of analyses (A-D above; analysis E imental sensu Doyle & Donoghue (19a6b). The generated more equally most parsimonious trees basic philosophy of this approach was well sum- than PA UP 2.4 can store). In each case, an initial marized by Johnson (1982) and Bryant (1989: run used the BANDB command to find aU equally 218): "Parsimony determines the order by which most parsimonioyis topologies by branch-and-bound, viable hypotheses should be tested; one starts with and the combination of the OPT=MINF optimi- the simplest" (our italics). Alternative hypotheses zation algorithm and APOLIST print command to are then considered in order of increasing com- identify the putative location and direction of each plexity untQ a self-imposed threshold is reached. character state transition. Having thus determined In contrast, nonexperimental cladistic studies both the length of the shortest tree(s) (L„i„), we then start and finish with the simplest. reanalyzed the data matrix hy replacing the BANDB command with BB = 'X', where 'X' was one step SPECtES-LEVEL RELATtONSHtPS longer than the shortest tree (i.e., L^+i). This second run found and saved trees of lengths L^, Although this experimental cladistic study was and L^,+i; in order to determine the number of aimed primarily at elucidating genus-level relation- topologies of length L^+^, the total number of ships, we chose to perform our analyses at the topologies found at BB = L„i„ was subtracted from species level. This decision partly reflected a sub- the total number of topologies found at BB = L„i„.^i. sidiary interest in species-level relationships, but This procedure was repeated up to lengths of about was taken primardy because species-level OTUs L„i„+, (depending on the particular submatrix under provide a test of the presumed monophyly of gen- scrutiny). Tree number increases, mo re-or-less ex- era. Genera can then be re-delimited if necessary. ponentially with increase in length; the maximum The foEowing discussion is based primarily on anal- capacity of PAUP 2.4 to store trees (N = 100) is ysis A, but also applies to analyses B-D (analysis soon exceeded, so that it becomes untenable to E produced an untenably large number of equally routinely scrutinize topologies much longer than most parsimonious trees). Only four of the ten genera in the data matrix We found such scrutiny desirable for two rea- are represented by more than one OTU (Table 1): sons. First, we wished to know how many genus- Sigillaria (two species), Diaphorodendron (three level topologies occurred at each length, as opposed species), Sytichysidendron. (two species), and Lep- to species (OTU-)level topologies routinely detect- idopkloios (three species, but see Appendix ID). 526 Annals of the Missouri Botanical Garden

105 > Paurod0!idron miponm (93 36 93 101 103) ^y 10/^ Oxfoadia gmcitis/sp. nov. (77 9S 97) 1,5 / «<= iir y^ / 112 Anabathra pulchemms / _ioa^/ (49 99 104) -^ 66 >X / !/^ ^v Chatofieria cermosa /^ / ^vr (5 3 21 24 92 102) y^ / _*«/^ / / 13/ / / 10 / SigWaria approx'sinata / X / ,x (99 91) / / ~^^/\t / / _107 / —•'X Sigitlaria&p. nov. / / 32 / „1«> ^ / / 71 / 35 / / —• X 'Hypothetical Ancestor' Diaphorodandfun sctarotkum ;s 11 12 iS 32 37 53 75] / / 53/ "^N/ W ' / -50/ M / / ^*/ XV / 40 y' 4S y^ i^ Diaphorodendran vasculara / -27/ _^^ / \ (*) / 6/X: \^ / 79 jt *\ Dlaphorod6ndiort phitlipsii 1 2 3 1S 22 23 2S 61 / 56 11-4 / X / sa_LiOv^ \ (36) 41 107 /• V 33 94 / X 33 GO 73' — / -74 X y 35 38 / 77— X * / Synchysidendron sp. nov. -1S_66/' •" \X (IS 34) 51 S3 72 7+ 76 81 / 20 X / 17 -33 \ Synchysidendrcn dicontrioum £4 SS 57 60 SO / (19)

\ .54^-Z.V Hiiemodandtson serratum X -33 -73 X \ :i~Z? / (*) X, M 86 / 3 loa 112 'X -^Z jj , Lepidodendron hickii X, y -33 /^ (43 73) x^ /^ ^y^

\/ /^ -112 Lspidophlaios harcouriii _\. / -108 / •23 39 47 43 53 e2 ee 70 >/ 105 >^ (*)

25 28 52 -S? 64 64 \/ , / Lspidophloios johnsanii ^^C /'^ IB X/ <*)

-47 -103 \ Lepidophtoios hallii (65) FIGURE 6. Preferred most psrsimonious cladogram for analysis A (all OTUs and all characters). Holapomorphies are placed in square brackets below the hypothetical ancestor, and autapomorphies are placed in parentheses below OTUs; all character state transitions on terminal branches are therefore homoplastic. Characters that experience reversal are underlined (with a minus sign where a reversal occurs), parallelisms arc ovcrlined. Asterisks indicate absence of character state transitions at specific nodes.

Each of these four genera proved very robust (i.e., dcum is very poorly resolved (Fig. 6), resting en- dismantling each genus in any way resulted in much tirely on the nonhomoplastic synapomorphy of longer trees), hut relationships of the species within secondary xylem in lateral branches (C30) that at least two of the genera are less clear (the two unites D. sderoticum and D. vascnlare {Fig. 8d). species of Sigillaria and SynchysidenAron re- Treating C30 as a synapomorphy of the clade and spectively do not allow multiple topologies). as a secondary loss in D. phillipsii- (a tenable The three-taxon problem presented by Dtapko- hypothesis more consistent with stratigraphic evi- rodendron pkUUpsii, D. vasculare, and D. sclero- dence; Fig. 3) costs only one extra step and col- Volume 79, Number 3 Bateman et al. 527 1992 Arborescent Lyoopsid Phylogeny

ffi Paurodendron traipomli (93 96 98 101 108)

Oxroadia gracilis/sp. rov. (77 95 97)

Anabathra pulchomma (49 99 104]

Chahit6fia cormosa (5 9 21 24 92 102]

Sigillaria appmximala (89 91]

Sigillaria sp. nov. (•)

DIaphorodendron sclerotlcum 'Hypothetical Ancestor' [8 11 12 29 32 37 S3 7S! (4)

Dlaphorodendron vasculare (*)

Diaphorodandran phlUipsll (3S) 1 a 15 22 23 26 61

Synchysidandmn sp. rov. 33 El 63 72 73 74 76 aO ai 90 (IS 34)

Synchysidandron dicentrioum (19)

Hizamadandron serraium (*)

Lepldodendmn hickii (46 78)

Lapidaphloias harooutlii (•) 2S -26 2a 4^ E2 S3 £4 63 76 64 Lepidophloios johnsoe^i (*)

Lapidophloios hattii (65) FIGURE 7. Fully annotated cladogram for analysis A showing alternative generic topologies of potential interest. It differs from Figure 6 in that (1) Paurodendran is a sister group of Oxroadia (cost = two steps)^ (2) Anabathra and Chaloneria form a clade (cost = nil). (3) SigHlari/L and Diapkorodendron form a clade (cost = one step), and (4) Hizerruidendron. and Lepid,odendron sens. str. form a clade (cost = five steps). Character notation follows Figure 6.

Lapses the relationship into an uninformative tri- idophloios kalUi and L. harcourdi are subtended chotomy (Fig. 8e). This poLychotomy was a only hy homoplasies, while L. johiisoriu is not persistent cause of trivially multiple topologies in subtended by any characters (it even lacks quali- our analyses (see Appendix 2). tative autapomorphies; Fig. 6). We obtained three The phylogenetic relationship of the three pu- equally most parsimonious solutions to this three- tative Lepidophloios species is obscured by exten- taxon problem {Fig. 8a-c). The first (Fig. 8a) links sive homoplasy that is compounded by ambiguities t. johnsonii and L. hallii by the homoplastic syn- caused by missing values for some characters. Lep- apomorphy of a filamentous core to the protostele 528 Annals of the Missouri Botanicai Garden

(C16). The second (Fig. 8b) links h. johnsonii and L. harcourtii by the homoplastic synapomorphy of a glandular periderm (C47) and by the ostensibly nonhomoplastic synapomorphy of arched leaf cushions (C64). Unfortunately, this character is scored as missing for L. hallii as a result of X-coding (Table 3) and can therefore be treated as either apomorphic or plesiomorphic during optimization. 25 28 52 -67 64 8+ As a result of inconsistent replacement during optimization, the apomorphic state is depicted as characterizing all three Lepidopkloios species in Figure 8a but only two species in Figure 8b. The HL JO HC (65) <^ third topology (Fig. 8c) treats C16 as a loss in L. harcourtli and C64 as present in all three species, which consequently coUapse to a trichotomy. -103-Ny *'^\ / Given that aU three solutions are equally most -109 parsimonious, every topology that differed in the ^\ X— -112 \ /^47 positions of OTUs other than LepidophloLoi spe- V 64 cies was repeated three times by the tree-building algorithm to accommodate the multiple solutions y^25 28 52 -S7 84 to the Lepidapkkiios problem (hence our division hy three of the algorithmicaUy determined numbers of species-level topologies to yield the smaller, more JO HC HL meaningful values listed in Table 4). The arrange- (65) (*) (•) ment of Lepidopkloios species shown in Figure 8a -16 \ / best fits their reported sequence of relative ap- \ - - 105 -/..I pearance in the fossil record (Fig. 3); on the basis * \ -109 / -103 -112> of this weak evidence, it was preferred when selecting the trees shown in Figures 6 and 7.

EXPERIMENTAL CLADISTICS: A SURVEY OF '25 28 52 -67 64 84 GENUS-LEVEL TOPOLOGIES In all analyses, Synckysidendron and Diapho- roderidroii sens, str, consistently remained united as a monophyletic group and are not distinguished in Figures 9 and 10, Also, the following discussion occasionally refers to SynckysLdendrofi as derived relative to Diapkorodendron and Lepidopkloios as derived relative to Lepidodendron. As these pairs of genera are sister groups (Fig. 6), these assertions of derivation are subjectively imposed by us, based on comparison of the number and inferred evolutionary signiftcance of the character 6 7 42 45 state transitions supporting each genus.

FIGURE 8. Poorly resolved relationships iaetween species of the same genus (see caption to Table 3 for key to abbreviations). 5.-C show three equally parsimonious (12- step) solutions to the three ta.xon problem presented by the Lepidopkloios species, d and e show two solutions to the three taxon problem presented by the Diaphorod^n- d-Ton, species (d = 7 steps, e = 8 steps). Notation largely follows Figure 6, though hnes below character numbers 7 30 42 45 emphasizing reversals are omitted. Volume 79, Number 3 Bateman et al. 529 1992 Arborescent Lyoopsid Phylogeny

^ fl) D O 41 • •^ c '^ to ^ *3 I I I [ I u W o >0 >iD M CT- « O Si to HE (N Tji '73 ^ 4:1 '3 1) 'S ^ '43 ~ s > 4:1 u 4> 'a u

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SY PN ox AN CH SI Dl HZ L^ LS AN CH CH m

SY SY SY ox PN SI Dl AN CH SI Dl CH A^ SI Dl

PN OX AN CH PN OX CH m OX PN CH AN

AN CH SI PN OX AN CH SI Dl SY HZ LN LS

FIGURE 9. Generic topologies of analysis A at L^ (a-c) and L^+i (d-k) (see caption to Table 3 for key to abbreviations). For analysis B (babit cbaracters omitted), a and b occur at L^,, and c-f, b at L^+i (tbe relationsbip between Chaloaeria. and Anahatkra became unresolved in c). For analysis C (Chaioneria omitted), only single generic topologies occur at L^ (that seen in a-e less Ckaloneria) and at h„i^^.^ (that seen in e-g). 1 is a strict conaensua tree for analysis A at L^+j, analysis B at L^+j, and analysis C at L^+, (less ChaloneHa). Synckysidendron and Diapkorodendron. are not distinguished in Figures a-g as tbey consistently behave as sister groups. All character information is omitted.

Analysis A (all OTUs and all characters includ- and is united with Anabathra to form a mono- 'ed) . Analysis A yielded three equally most parsi- phyletic clade in the third MPT (Fig. 9b). monious trees (MPTs; Fig. 9a-c) that unite Decreasing the level of parsimony by addmg one Oxroadia and Pauradendron as a basal clade. The step (L^^-i) yields another eight generic topologies preferred most parsimonious tree (PMPT) depicts (Fig. 9d—k). Three of these unite Sigillaria with the remaitiing genera as a perfectly nested se- Diaphorodendron—Synckysiden.dron (Fig. 9e-g), quence of increasingly apomorphic OTUs (Figs. 6, otherwise repeating the three possible relationships 9a). The three MPTs differ in the position of Ckal- between Chaioneria and Anabathra seen in Figure oneria, which occurs immediately above Anabath- 9a-c. Four others dissociate the Oxroadia-Pau^ ra in the preferred MPT (Fig. 9a), immediately radendron clade, so that each arises directly from below Anabatkra in the second MPT (Fig. 9c), the major axis (Fig. 9d, h-j); three of these (Fig. Volume 79, Number 3 Bateman et al. 531 1992 Arborescent Lycopsid Phylogeny

9h-i) also involve changes in the relative positions tree, between Oxroadia—Paurodendron and An- of Anahatkra and Chaloneria. It is then equaQy ahatkra, or it can be appended to Anahatkra to parsimonious to have Oxroadia (Fig. 9(1, j) or yield a more innovative topology. Paarodendron (Fig. 9h, i) as the basal OTU of the A strict consensus tree (Nelson, 1979, 1983) tree. The eighth topology unites Sigillaria and at L^+.^ (analyses A, B) or L„i,+j (analysis C), has Ckaloneria, linking both to Anahatkra to form a only four nodes (Fig. 91); only Oxroadia and Paix- substantially different topology (Fig. 9k). rodendron (at the base of the tree), Diapkoro- At L„;„^_l, some topologies unite Ckaloneria and dendron and Synckysidendron, and Lepidoden- Sigillaria, others allow the exchange of Hizemo- dran and Lepidopkloios (at the apex) are dendron and Sigillaria. across Diaphorodendron— consistently conjoined and/or juxtaposed. Synckysidendroa (cf. Fig. 9a). The putative Sig- Analysis D (all OTUs, vegetative ckaracters illaria-Diap korodendron-Sync hys idendron clade only) . The preferred MPT for analysis D (Figs. can be placed above Hizemodendron.. Alterna- 10a, 11) is pectinate (each genus is connected tively, placing Ckaloneria immediately below An- directly to the major axis) and differs substantiaQy ahatkra allows the Sigillaria—Diaphorodendron— from the preferred MPT of analyses A-C (see also Synchysidendron clade to be situated between or Bateman & DiMichele, 1991). Lepidodendron and immediately below these genera. Together, the five Lepidopkloios remain linked at the top of the tree, genera can form a sister clade to Hizemodendron- but two pairs of adjacent branches are transposed Lepidodendron—Lepidopkloios, either with Ckal- {Sigillaria and Diapkorodendron-Synchysiden- oneria—Anahatkra and Sigillaria—Diaphoroden- dron, Anahatkra and Ckaloneria). The Oxroad- dron-Synckysidendron as sister groups or as a ia-Paarodendron clade.is split into its constituent nested clade {({(Diaphoradendron-Synckysiden- genera, each of which forms an equally parsimo- dron) Sigillaria) Anahatkra) Ckaloneria), nious sister group to the rest of the ingroup (Fig. Analysis B (all OTUs, "kabit" characters Cl— 10a, b). Hizemodendron is sister group to the most C7 omitted) . The two MPTs of analysis B are derived genera Lepidodendron and Lepidopkloios identical to two of the three MPTs of analysis A in the preferred MPT of analysis A (Fig. 9a), but (Fig. 9a, b). Five additional topologies occur at is derived relative only to Oxroadia and Pau.ro- Lmn+Li one fails to resolve the relationship between dendron in the preferred MPT of analysis D. Ckaloneria and Anahatkra (dashed line on Fig. All of the variation among the eight additional 9c), two unite Sigillaria and Diapkorodendron— generic topologies at L^in^-i occuLrs tielow Diapko- Synckysidendron (Fig. 9e, f), and two allow dis- rodendron-Synckysidendron in the tree, indicat- sociation of the Oxroadia—Panradendron clade ing that the more appmorphic portion of the tree (Fig. 9d, \i). At L^+j, Ckaloneria can be united is the most robust. An unresolved trichotomy re- with Sigillaria, Hizemodendron and Sigillaria places the Oxroadia-Paurodendron clade (Fig. can be transposed across Diapkorodendron—Syn- lOc). The remaining topologies place Anahatkra ckysidendron, and the putative Diapkoroden- below Ckaloneria (Fig. lOd-f) or unite Anahatkra dron—Synckysidendron—Sigillaria clade shown in and Ckaloneria as a separate clade (Fig. lOg-j). Figure 9e can be placed above Hizemodendron or Hizemodendron is the least stable genus; it can below Anahatkra and Ckaloneria. AU topologies occur below (Fig. lOa-e, g, i) or above (Fig. lOf, found in analysis B at L^^+j were also found in h, j) Anahatkra and Ckaloneria. In the most rad- analysis A at h„-^+^. ical topology, Hizemodendron is the sister group of Anahatkra and Ckaloneria, together forming Analysis C (Ckaloneria omitted, all ckaracters a separate clade (Fig. I Ok). included) . The only MPT from analysis C merely deletes Ckaloneria from the preferred MPT of Analysis E (all QTUs, reproductive ckaracters analysis A (Fig, 9a). Increasing the.number of steps only) . In contrast with the other analyses, it was aQow a Sigillaria—Diapkorodendron-Synckysi- not possible using PALTP 2.4 to store and thereby dendron clade, either below (L^.^) or above (L^+j) screen all 810 MPTs for analysis E (270 trees, if Hizemodendron, and disaggregation of the the equally most parsimonious solutions to the Lep- Oxroadia—Panradendronc\&(ii,(L,^.^2)- The range idopkloios species relationships are ignored). of topologies substantially increases at L^+j. Once AvaUable evidence suggests that the number of again, Sigillaria and Hizemodendron can be ex- MPTs was grossly exaggerated by repeated poly- changed across Diapkorodendron-Synchysiden- chotomies and conceals a much smaller number of dron. A putative Sigillaria-Diapkorodendron- substantially different topologies. A representative Synchysidendron clade can be placed low in the and fully annotated MPT is shown in Figure 12a. 532 Annals of the MissQuri Botanical Garden

PN ox HZ CH AN ox PN

HZ AN CH OX P^ HZ AN CH OX PN AN CH HZ

HZ CH AN CH AN HZ OX PN HZ CH AN

OX PN CH A^ H2 CH AN HZ

FIGURE 10. Generic topologies of analysis D (vegetative characters only) at L^-^ (a, b) and L^,+i (c-k). (See caption to Table 3 for key to abbreviations.) Only those portions of trees that differ from the preferred most parainionious tree (a) are shown, and all character iiiforniation is onnitted.

Unlike analyses A-D, the relationship between the dient of this increase provides an estimate (albeit four most primitive OTUs is unresolved, as are the crude and dependent on matrix size) of the relative relationships between (1) the three species of Dia- resolution of different data matrices; more confi- phorodeadron. sens: st^., and (2) Hizemodendron dence can be placed on a most parsimonious tree and Lepidodendron. The most radical innovation from a matrix that yields few alternative trees of is the depiction of LepiddphLoios as polyphyletic; optimal or near-optimal length (more rigorous, sta- the relatively primitive L. hdrcoiirUL is separated tistical methods are now available for determining from L. johnsonii and L. kallii by Lepidodendron confidence limits of specific topologies; e.g., Fel- and Hizemodendroa. Restoring Lepidophloios to senstein, 1985; Archie, 1989b; Sanderson, 1989). monophyly costs one additional step (Fig. 12b). For our data, the complete data matrix (analysis A) provides a yardstick by which to measure the Methodological conclusions. For any cladistic ma- relative resolution of analyses based on selectively trix, progressive one-step increases in length rel- reduced permutations of the matrix presented in ative to the MPT result in a rapid increase in the Table 3 (i.e., analyses B-E). Omitting the five number of topologies obtained (Table 4). The gra- synapomorphic habit characters (analysis B) yield- Volume 79, Number 3 Bateman et al. 533 1992 Arborescent Lycopsid Phylogeny

. PNFH 10 ,

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FIGURE 11, Preferred moat parsimonious ciadogram for analysis D (vegetative chara.cters only). Character notation follows Figure 6, OTU notation follows Table 3.

ed fewer topologies of length L^;.-L^+1 and slightly E yielded 270 equally most parsimonious trees, aU increased the consistency index (Table 4). Omitting containitig at least one polychototny. Thus, it is Chaloneria^ the least stable OTU (analysis C), in- tempting to argue that vegetative characters are creased the consistency index by a similar amount more phylogenetically informative (i.e., less ho- to that of analysis B and generated an even more moplastic) than reproductive cha.racters, but levels highly resolved set of trees that included only one of homoplasy are very similar in the MPTs of the most parsimonious topology (Fig. 9a). vegetative and the reproductive aubmatrices (con- Substantially reducing the size of the data matrix sistency index values = 0.66 and 0.67 respec- analyzed by including only vegetative characters tively; Table 4). Rather, the crucial difference ap- (analysis D) or only reproductive characters (anal- parently lies in the different sizes of the suhmatrices, ysis E) also increased consistency index values rel- which are reflected in different values for the av- ative to those of analysis A. However, in contrast erage number of synapomorphic character states with analyses B and C, analyses D and E yielded per OTU: 3.2 in analysis D and 1.8'in analysis E. less resolved sets of topologies (Table 4). Analysis For the preferred MPT of our complete matrix, D provided acceptable results (Fig. 10), but analysis the number of steps per synapomorphy (1.6) and 534 Annals of the Missouri Botanical Garden

ANPU 106 >:^ (99 <(14)

CHCO * j^ J^ (5 92 102) * / SIAP y (69 91) /lOoN SINS (*) *./ DISC (*) / /\ DIVA x (*) X DIPH {*) 74 IS S< 82 iin ^ *./ SYNS V {*) X SVDI (5»)

ios . LSHC fli j/ (*)

-ii 63 45 07 roa IM -IO7' y '74 y Hzse '73 y( (*) /* ^ LNHf P^ (76) LSJO {*)

-ioa'\ LSHL (*)

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b LSHL FIGURE 12. a. Preferred most parsimoniooa cladogram Tor analysia E (reproductive characters only). Character notation follows Figure 6, OTU notation follows Table 3.—b. Terminal portion of an alternative topology at L^+i. the resulting corLsistency index (0.63) are average EMPIRICAL SUPPORT FOR ALTERNATIVE HYPOTHESES relative to those of other cladistic data matrices OF (JENERIC RELATIONSHIPS containing similar numbers of OTUs (the main variable influencing consistency index values: cf. The relative merits of the topologies described figs. 2a and 3 of Archie, 1989a- fig. lb of San- above are best assessed by examining the optimized derson & Donoghue, 1989). Thus, we suggest that distributions of character state transitions across for a data matrix of average homoplasy (as here), the trees and subjectively estimating the probabil- there is a threshold of minimum empirical support ities of alternative evolutionary scenarios for par- (2-3 synapomorphies per OTU) below which well- ticular suites of characters. To this end, many of resolved sets of fully dichotomous trees cannot be the near-optimally parsimonious pairings of genera expected (see also Felsenstein, 1985; Guyer & obtained during the topological survey of analysis Slowinski, 1991). A are summarized in a single fully aiuiotated tree Volume 79, Number 3 Bateman et al. 535 1992 Arborescent Lycxjpaid Phylogeny

(Fig. 7), to enable comparison with the preferred be fabe if the V-shaped leaf trace of Sigillaria moat parsLttionious tree (Fig. 6). reflects origination from two protoxylem strands, and the abaiial grooves may be develop mentally QxroaAia and Paurodendron. Oxroadia and Pau- related to leaf trace morphology. Anabatkra is rodendron. share orJy two synapomorphiea (Fig. united with Ckaloneria and Sigillaria on the basis 6). Both are nonhomoplastic and describe echinate of two homoplasies reflecting habit: the trunk pos- distal and proximal surfaces of microspore exinea sesses an apex that shows little if any branching (Clll, C115). Disaggregating this clade jiiducea (C3) and bears lateral branches and/or cones (C6; paraUelistti wi these characters, at the cost of one a character that could not be coded for the branch- step (Fig. 7). Given that echinate microspore exuies less and coneless Ckaloneria). Both states also could be regarded as a single character, the status characterize Diaphorodendron (Fig. 6). of these two genera as a monophyletic group may be even less well supported than parsimony sug- Diapkorodendron and Synchysidendron. The gests. A phylogenetic study focusing specifically on distinction between the segregate Synchysiden- these and other similarly primitive genera is re- dron {S. dicentricum. and Synckysidendron sp. quired to resolve this ambiguity. nov.) and the three species of Diaphorodendron sens. str. is well supported (Fig. 6), the former by Anahathra and ChaLoneria. Topologies treating seven synapomorphies (four nonhomoplastic) and this group as paraphyletic (Fig. 6) or as a mono- the latter by four synapomorphies (two nonhomo- phyletic clade (Fig. 7) are equally parsittionious, plastic). These characters, which represent habit differing orJy in the distributions of a few homo- sens. lat. (C3, C6-C7, C74), leaf base retention plasies. When united, the genera possess only two (C44-C45), stele histology (C17, C20, C31), and synapomorphies: weakly branched or unbranched periderm histology (C42-C43), reflect two sub- trunk apex (C3) and acutely angled leaf attachment stantially different growth hahits (see Evolutionary (C66). Both characters are parallelisms: trunks with Patterns). Nesting Synckysidendron within Dia- little or no branching are depicted as homoplastic, phorodendron requires a minimum of four extra also occurring in Sigillaria and Diaphoroden.- steps in analyses A, C, and D, and three extra dron. Angle of leaf attachment, a character prone steps when habit characters C1-C7 are omitted to ontogenetically related variation and ecopheno- (analysis B). Placing the genera on- separate ter- typic modification, is represented as a parallel trait minal branches is even less parsimonious. Although in Paurodendron. &nd Hizemodendron. Thus, ev- there is Uttle doubt that Diapho^rodendron sens, idence for an Anabathra-CkaLoneria clade is weak. lat. (i.e., sensu DiMichele, 1985) is monophyletic, Uniting Anabathra and Ckaloneria affects op- we believe that the differences between the two timized character state transitions elsewhere in the monophyletic groups of species that it contains are tree. In Figure 6, unbranched trunk apex (C3) is sufficiently profound to warrant segregation of the perceived as reversed in SynchysiAendron. and in new genus, Synckysidendron (Appendix IC). the Hizemodendron-Lepidodendran-Lepido- phloioi clade, but in Figure 7 this character state Sigillaria and Diaphorodendron-Synchysiden- is depicted as a parallel acquisition in Anabatkra,- dron. Sigillaria and Diaphorodendron-Syncky- Chaloneria, Diaphorodendron, and Sigillaria. The sidendron are empirically the best supported of all absence of a ligule cavity (C60) in Anabathra is the clades under scrutiny; .Sigillaria is supported a plesiomorphy in Figure 6 but a reversal in Figure by 14 characters (six nonhomoplastic), and Dia- phorodendron-Synckysidendron by 15 charac- 7. Missing values for C33 (secretory jntracortical leaf sheaths) and C73 (branch gap associated with ters (nine nonhomoplastic). Uniting Sigillaria with Diapkorodendron-Synckysidendron adds only peduncle) in Ckaloneria allow these characters to one step and transforms two reproductive char- be optimized as apomorphic in Figure 6 (despite acter states from parallelisms into nonhomoplastic the absence of a cone in ChaLoneria) but plesiomor- synapomorphies: short, horizontal alations on the phic in Figure 7. megasporophyll pedicel (C82), and crassitude mi- Anabathra, Ckaloneria, and Sigillaria. In anal- crospore laesurae (C107). Balancing these gains,- ysis A, these genera formed a clade at L^,.j,i (Fig. homoplasy is induced by losses in three character 9k). Ckaloneria and Sigillaria are united by two states: the presence of a lower keel on the leaf nonhomo plastic character states, fusiform rootlet cushion (C55), germination of megaspores within gaps (C13) and V-shaped leaf traces (C69), and the sporangium (C80), and reduction of viable by the homoplasy of abaxial grooves in the leaf megaspores to one per sporangium (C90, a logical (C70). The apparent synapomorphy for C69 may functional correlate of CSO). Although Figure 7 536 Annals of the Missouri Botanical Garden

portrays these character state transitions as re- of infrafoliar parichnos from a nonhomoplastic syn- versals in SigiUaria., they are more likely to rep- apomorphy of Lepidodendron and all Lepido- resent parallel acquisitiorLs in Diaphoroden-dran.— phloios species (Fig. 6) to a parallelism of Lepi- Synckysidendron and in the more derived Hize- dodendron and Lepidophloios hallii only (Fig. 7). modendron.- Lepidode ndron-Lepidap kioios clade Similarly, a missing value in Hizemodendron for (loss of these traits in SigiUaria, would probably multizoned periderm (C39) allows the genus to be confer a severe competitive disadvantage). As ali plesiomorphic for this character in Figure 6 but five of the above characters are considered poten- apomorphic in Figure 7. tiaEy homoplastic, the possible monophyly of Slg- However, the most deleterious consequence of iUaria-Diapkorodendron—Synchysidertdron re- uniting Hizemodendron and Lepidodendron is the mains equivocal. generation between Lepidodendron and Lepido- Differential optimization alters perceptions of phloios of five vegetative paraUehams: discernable evolutionary patterns of three other characters in protoxylem ridges on the stele (C26), resinous peri- Figure 7. The first is stem apical branching (C3, derm (C48), tangentially elongate leaf cushions on already discussed under Chaloneria-Anahathtd), twigs (C53), and a leaf with a dorsiventrally flat- and the remaining two describe leaf cushion mor- tened vascular strand (C68) and lateral abaxial phology. In Figure 6, the plicate lower field (C57) grooves (C70). The overaQ cost to parsimony (five evolves below Diapkorodendron—Synckysiden- steps) appears sufficient to reject the hypothesis of dron, and is subsequently lost in Lepidophloios, monophyly. Nevertheless, treating these hypoth- whereas in Figure 7 it is represented aa a paraEel esized character state transitions as reversals in acquisition in Diaphorodendron-Synchysiden- Hizemodendron suggests a heterochronic evolu- dron, Hisemodendran, and Lepidodendron. Sim- tionary mechanism that could allow monophyly (see ilarly, in Figure 6, the upper keel evolves below Evolutionary Patterns). Diaphorodendron—Synckysidendrort and is lost in Lepidodendron sens, lat. Prior to the studies of Hisemodendron., whereas in Figure 7 it evolves DiMichele (1985), Bateman & DiMichele (1991), below the Oxroadia-Paurodendron. clade (despite and DiMichele & Bateman (1992), 'Lepido- the absence of leaf cushions in these highly ple- dendron' sens. lat. encompassed four of the siomorphic genera) and is independently lost in anatomically preserved genera analyzed by us: SigiUaria and Hizemodendron. For both char- Lepidodendron sens, str., Hizemodendron, Dia- acters, the optimizations in Figure 6 are more phorodendron, and Synchysiden&ron. Forcing intuitive. these four genera into a single clade representing the traditional concept of Lepidodendron {not Q- Hizemodendron and Lepidodendron. As depicted lustrated) cost nine additional steps and revealed in Figure 6, the branches immediately subtending only one synapomorphy uniting the clade: a plicate Hizemodendron and Lepidodendron, share only lower field to the leaf cushion, which is reversed one character state transition: the loss of secretory in Lepidophloios in the preferred MPT (Fig. 6). intracortical leaf-trace sheaths (C33). The other In contrast, five nonhomoplastic synapomorphies four characters that support the Hizemodendron- in Figure 6 are rendered homoplastic: short, erect Lepidodendron clade in Figure 7 are aU parallel- megasporophyll alations (C83) and bilaterally flat- isms. Three describe microspore equatorial (CI03) tened (C85), distaliy dehiscent (087) megasporan- and contact face(C109, Cl 12) ornamentation and gia are lost in Diaphorodendron—Synckysiden- are homoplastic among Lepidophloios species. dron, and zoned periderm (C39) and infrafoliar Their frequencies and distributions differ between parichnos (C62) become parallelisms in Lepido- topologies, due to inconsistent optimization of miss- dendron and some Lepidophloios species as a ing values. These characters are more appropri- result of, ambiguous missing values in the latter. ately treated as reversals within Lepidophloios Moreover, homoplasy is increased in other char- (Fig. 6) than as paraQelisms in Lepidophloios and acters already depicted aa homoplastic in Figure Hizemodendron-Lepidodendron (Fig, 7). In Fig- 6. We conclude that ^Lepidodendron'' sens. lat. is ure 6, the fourth character state, phcation of the clearly a paraphyletic group. lower field of the leaf cushion (C57), originates below Diaphorodendron-Synchysidendron and is MULTIVARI/VTE ANALYSIS reversed in Lepidophloios. In Figure 7, this character state originates twice, in Diaphorodendron- In order to examine patterns of morphological Synchysidendron and in Hizemodendron (a less variation free from the rigid constraints imposed probable scenario). Missing values allow demotion by cladistic nested hierarchies, we subjected the Volume 79, Number 3 Bateman et al. 537 1992 Arborescent Lycopsid Phytogeny

cladistic data matrix (Table 3) to multivariate anal- • SYDI ysis. A value of zero or unity was substituted a priori for each missing value according to optimized distributions of character state transitions in the SINS preferred most parsimonious cladogram (Table 3 subscripts, Fig. 6). The resulting uniformly binary matrix aQowed generation of a symmetrical matrix comparing OTUs without a priori standardization, simply using the number of character state conflicts (i.e., 0 vs. I) aa a direct measure of dissimQarity between pairs of OTUs. The dissimilarity values were used to construct an unrooted minimum spanning tree (Gower & Ross, 1969); links in the tree represent specific sets of character state transitions, thus contradicting frequent assertions that phenetic

trees inevitably lack such information. Also, prin- LSHL cipal coordinates (Gower, 1966) were calculated / from the data matrix via Manhattan distances, SINS Hzse- -LSJO \ using unpublished software written by J. Alroy. LSHC Holapomorphies (which are invariant) were ex- A \ cluded (as in cladistic analysis), but autapomorphies PNFR eHCQ contributed to both the unrooted tree and the ordination. Links between genera on the minimum spanning FIGURE 13. a^ Minimum spanning tree (unrooted phe- tree (Fig. 13a) represent at least 10 character netic tree) aa based on cladiatic data matrix (Table 3, q.v. for key to OTUs). Links represent numbers of character conflicts, those within genera represent no more state conflicts. — b. Alternative links that are almost max- than five. The 21 conflicts between Hizemoden- imally parsimonious; additional steps relative to a are dron and Lepidodendron, and 14 conflicts be- marked. tween Synchysidendron. and Diapkoroden-dron., emphasize the need to segregate these new genera putatively more derived Synchysidendron giving (Appendix IC). rise to the more primitive Diaphorodendron. Pau.- The minimum spanning tree resembles the pre- rodendron can replace Oxroadia as the closer ferred most parsimonious cladogram (Fig. 6) in relative of Anahathra at the cost of one step. depicting a progression from Paarodendron and In summary, the phenetic trees serve primarily Oxroadla through An.aba.tkra, Hi.zemoden.dron., to emphasize the potentially pivotal role of Ana- and Lepidodendron to Lepidopkloios (though L. bathra as the most primitive arboreous lycopsid johnsonii is shown as ancestral to the two remain- analyzed. ing species). However, Anabathra is also depicted The first three principal coordinates (Fig. 14) as the ancestor of a second lineage, consisting of account for an unusually large proportion (91%) Chaloneria, SigiHaria, Diapkorodendron, and of the total variance. The first coordinate separates Synchyside.ndrQn,, that is not represented among Diapkorodendron-Synchysidendron, from the the range of cladograms shown in Figure 9. This other genera, the second coordinate separates Lep- second lineage is held together by the weakest links idodendron-Lepidophlotos from the bisporan- in the tree iChaloneria—Sigillaria = 29 conflicts, giate-coned group of Paurodendron-Oxroadia- Sigillaria-Diapkorodendron, = 33 conflicts) and Anahatkra-Ckaloneria (with Hizemodendron in- consequently can be dissociated at the cost of very termediate), and the appreciably weaker third co- few additional steps (Fig. 13b), demonstrating that ordinate sepai-ates Sigillaria (and, to a lesser ex- these genera are the most problematic in both the tent, ChaLoneria) from the remainder. The resulting cladisticaUy and phenetically generated phyloge- tetrahedral arrangement of four clusters (excluding nies. Attaching Sigillaria directly to Aiiabatkra, Hizemodendron), separated by broad morpholog- rather than via Chaloneria, creates an intuitively ical discontinuities, underlines the distinctiveness more credible evolutionary hypothesis at the ex- of the three groups of monosporangiate-coned trees pense of two steps. Diapkorodendron and Syn- {Sigillaria, Diaphorodeiidron-Synckysiden- ckysidendron can be attached to HLzemodendron dron., Lepidodendron-Lepidopkloios) and the at the cost of only one step, but this results in the consequent difficulties of resolving their phyloge- 538 Annals of the Missouri Botanical Garden

relative to Dio-phorodendron-Synchysidendron. The genera whose positions differ most between the reproductive and vegetative dado grams are the bisporangiate-coned tree Anabatkra, which is reproductively plesiomorphic and vegetatively apomorphic, and the monosporangiate-coned pseudoherb Hizemodendron, which is reproductively apomorphic and vegetatively plesiomorphic (see also Bateman & DiMichele, 1991). Thus, monosporangiate cones (Fig. 12) and the tree habit {Fig. 11) cannot both be nonhomoplastic, though a fuU analysis using vegetative and reproductive characters together could have yielded a compromise solution involving homoplasy in both suites of characters. In fact, although its topology FlCURE 14. Principal coordinates ordination of the OTUs, based on Table 3 (q.v. for OTUs). Only genera differs in detail from those of analyses D and E, are labeled. Two Diapharadendron species are indistin- the preferred MPT for analysis A (aQ characters guishable on the flrst three coordinates. and OTUs; Fig. 6) more closely resembles the exclusively reproductive cladogram (Fig. 12) than the exclusively vegetative cladogram (Fig. 11); in netic relationships relative to each other and to particular, the monosporangiate-coned clade is re- Anaba.thra, their most hkely aiater group. tained at the expense of depicting the tree habit as homo plastic. EVOLUTION/VRY PATTERNS AND PROCESSES The two subsections that foEow discuss in greater Overall trends. Much of the variation among ar- detail the reproductive and vegetative trends, fo- borescent lycopsids can be resolved into a vege- cusing on the functional morphology and adaptive tative trend, reflecting in particular morphological {or nonadaptive) significance of specific character and anatomical expression of different growth ar- states, before returning to the evolutionary impli- chitectures, and a reproductive trend, representing cations (and limitations) of the preferred whole- increasingly sophisticated reproductive strategies. organism cladogram. The phylogenetic analyses show that the two trends are not entirely concordant; the preferred MPTs Reproductive morphology. Reproductive char- using vegetative characters only (analysis D; Fig. acters proved to be of little value in elucidating 11) and reproductive characters only (analysis E; phylogenetic relationships within the plesiomorphic Fig. 12) have substantially different topologies. The group of bisporangiate-coned OTUs, which differ following discussion of these trends emphasizes primarily in autapomorphic spore character states characters for which we developed strong (often a (Fig. 12). Careful revision of bisporangiate cones priori) hypotheses of high burden and pays partic- is desirable, to search for potential synapomorphies ular attention to the relative temporal order of less inclusive than the entire group. It is particu- appearance of apomorphic states of different char- larly important to understand the ontogeny and acters (e.g., Donoghue, 1989). reproductive biology of the bisporangiate cones in Many (possibly aQ) of the MPTs of analysis E order to determine how they could have given rise (reproductive characters only) distinguish the four to monosporangiate-coned descendants. All bispo- bisporangiate-coned genera (Paurodendron, rangiate cones have apically concentrated micro- Oxroadia, Anahathra, Ckaloneria) from the five sporangia and basally concentrated megasporangia relatively derived genera that possess a suite of irrespective of presumed geotropic orientation, sug- characters reflecting the developmental partition- gesting a shared developmental control of sporo- ing of mega- and microsporangia into monosporan- genesis. giate cones {Fig. 12). In contrast, the preferred In contrast, the functional morphology of re- MPT of analysis D (vegetative characters only) productive characters within the monosporangiate- distinguishes four primitive pseudoherbs/shrubs coned portion of the lepidodendralean clade has {PaiLfodeadron, Oxroadia, Hizemodendron, prompted much discussion (e.g., Thomas, 1978; Cha,lone.ria) from five derived arboreous genera Phillips, 1979; DiMichele & PhiUips, 1985; PhQ- (the derived clade is supported by the tree habit lips & DiMichele, 1992; see Appendix ID for the only:, Fig. 11) and depicts SigUlaria as derived taxonomic impfications). In Figures 6 and 12, the Volume 79, Number 3 Bateman et al. 539 1992 Arborescent Lyoopaid Phytogeny

appearance of monosporangiate cones (immediate- In particular, it allowed spatially independent de- ly below Sigillarla) is accompanied by lateral ex- velopment of the mega- and microsporophyUs, pansion of the aporophyll pedicel to form alations thereby permitting modifications of the megaspo- and by the functionally important transition in basic rophyU-megasporangium units that could have im- dispersal unit from isolated megaspores to the paired the function of micros porophy 11 units if sim- megasporophyll-megasporangium complex. All ilarly modified (a likely consequence in bisporangiate three character states persist without reversal cones, where mega- and microsporophyUs form a throughout the derived clade, indicating strong developmental continuum). Thus, free megaspores functional linkage that may be evolutionarQy tied were superseded as the basic dispersal unit by the to elaboration of the leaf bases. megasporophyU-megasporangium complex. Current evidence suggests that the leaf lamina The remaining reproductive modifications that and leaf base are derived from the same primor- delimit increasingly exclusive portions of the mono- dium; the leaf cushion, an elaborated leaf base, is sporangiate-coned clade can be envisioned as a also fundamentally foliar. Furthermore, we believe progressive evolutionary trend toward /i^-selection that the sporophyll lamina is homologous with the (sensu Pianka, 1970). Megaspores decrease in leaf lamina, and that the sporangium-bearing ped- number and increase in size, and the pediceUate icel is homologous with the leaf base, including an tissues surrounding the megasporangium become elaborated cushion if present. The strongest evi- adapted for increasingly specialized modes of mi- dence supporting these homologies is provided by crospore/microgametophyte capture and diaspore the ligule (e.g., Phillips, 1979; Bateman, 1988), dispersal (e.g., PhiUips, 1979). However, argu- which occurs adaxially on (Paurodendron) or with- ments that the most derived product of thia evo- in (all other OTUs) the bases of leaves (Fig. 4b) lutionary trend, Lepidophloios-Lepidocarpon, but on aporophylla occurs close to the distal end possesses true seeds (Zhang et al., 1986) are phy- of the pedicel, between the sporangium and the logeneticaUy unhelpful; the megasporophy 11s are more-or-less perpendicular junction of the pedicel clearly analogs rather than homologs of gymno- and lamina (Fig. 4d). Regarding the attachment of sperm ovulea. the ligule as a homologous point impUes that the Reduction in megaspore number to one per spo- pedicel is indeed homologous with the leaf base. rangium, and concomitant germination of mega- Both the leaf base (and thereby cushion) and lamina spores within the sporangium, distinguish the re- originate from the same primordium, as do the mainder of the monosporangiate-GOBed clade from sporophyU pedicel and lamina. Leaf and sporophyll Sigillaria. (Figs. 6, 12). The dichotomy immedi- both bear a ligule and both are fundamentally ap- ately above Sigillaria results in two clades well pendicular in origin. Moreover, there ia a strong supported by reproductive characters: Diapkoro- positive correlation between the complexity of the dendron—SynchysidendroTi. (proximaliy dehiscent, pedicel-sporangium unit and that of the leaf base; dorsiventraEy flattened, heteroceUular megaspo- definable leaf cushions appear at the same node of rangium containing gulate megaspores; granulate- the cladogram as monosporangiate cones, and both foveolate Granasporites microspores), and Hize- structures progressively increase in complexity moderidron,—LepLdoden.dron.-Lepidopklaias (dis- through the remainder of the clade, culminating in taUy dehiscent, cylindrical sporangium subtended the large, elaborate leaf cushions and equally large, by suberect alations; cingulate Lycospora micro- seedlike megasporophyU of Lepidophloios (e.g.. spores). Enveloping, integumentlike alations delimit Reed, 1941; Phillips, 1979). Thus, the evolution Lepidopkloios (Fig. 6; in the analysis of repro- of the leaf cushion may have been developmentally ductive characters only (Fig. 12a), this single char- linked to that of the sporophyll (T. L. PhUlips, pers. acter is insufficient to override differences in mi- comm. 1989). It is not clear whether elaboration cros pore ornamentation between Lepidophloios of the leaf prompted modification of the sporophyU, species, resulting in depiction of the genus as poly- or whether increase in size of the appendicular phyletic; inducing monophyly in Lepidophloios primordial meristems allowed simultaneous expan- costs one extra step (Fig. 12b)). Interestingly, the sion and elaboration of both leaf bases and spo- vegetatively well-differentiated species of Diapho- rophyU pedicels. rodendron and Synckysidendron (Fig. 11) are Whatever its driving mechanism, the transition effectively uniform in reproductive characters (the from bisporangiate to monosporangiate conea (im- meduUated stele attributed to Diaphorodendron mediately below Sigillaria on Figs. 6 and 12} (C74) strictly applies to the cone-bearing lateral represents a crucial release from developmental branches rather than the cones per se; Appendix constraints (cf Endresa, 1987, on angiosperms). ID). 540 Annals of the Missouri Botanical Garden

Distinguishing between, monoecious and dioe- ornamentation of Oxroadia megaspores by Bate- cious strategies is especially valuable in interpreting man (1988). The pseudosaccus of Chaloneria mi- the phylogeny and the functional morphology of crospores and cingulum of Hize-modendron., Lep- extant plants (e.g., Bawa, 1980; Givnish, 1980, idodendron, and Lepidophloios microspores 1982; Donoghue, 1989). Unfortunately, the al- probably acted as buoyancy aids. most inevitable disarticulation of cones from vegetative axes undermines attempts to identify the Vegetative morphology. Vegetative characters reproductive strategies adopted by members of the uniting the arborescent lycopsids are those asso- monosporangiate-coned lycopsid clade. Were in- ciated with the production of rhiaomorphs and wood, dividual plants monoecious or dioecious? If mon- together with Ugules and exarch xylem maturation oecious {as seems more likely), did megasporangiate (inferred centrifugal maturation in stigmarian rhi- and microsporangiate cooes mature synchronously zomorphs {Frankenberg & Eggert, 1969) is suspect or sequentiaQy? Or were arborescent lycopsids ca- (Phillips & DiMichele, 1992)). Beginning at the pable of even more complex strategies, such as root of the preferred MPT and passing along its gynodioecy? major axis (Fig. 6), the node above PanrodenAron- Overall, spore morphology proved less phylo- OxroaAia is characterized by the appearance of geneticaUy informative than cone morphology. the tree habit (habit is discussed more fully in Many of the spore character states are species- subsequent subsections) and by modifications to level autapomorphies, and the remainder exhibit vascular tissue that probably reflect greatly in- significantly greater homoplasy than cone char- creased body size: medullation of the stele, contin- acters (in Fig. 6, the proportion of holapornorphies uous protoxylem sheath, loss of protoxylem ridges plus autapomorphies and consistency index for cone (together causing superficial leaf trace emission: and sporophyll characters are 26% and 0.78 re- Fig. 5b), and the advent of foliar parichnos in the spectively, contrasting with values of 42% and leaf bases, now much more distant from the axial 0.64 for mega- and microspore characters). In vasculature following acquisition of the arboreoua retrospect, some cases of mistaken homology are habit. Beyond Anabathra, the ligule pit is ubiq- clearly evident among spore characters. For ex- uitous, though it also occurs in the ostensibly prim- ample, the distal spines (ClOO) of O^croadia and itive genus OxroadLa. Sigillaria sp. nov. megaspores differ in detail; those Beyond Chaloneria, the evolution of discrete of the former are Ipng and buttressed, those of the leaf cushions provided a consister^ basal limit to latter are short and almost papiUate, Also, polar- leaf atrophy. Many of the characters that support ization of spore characters was especially problem- nodes higher in the cladogram represent elabora- atic, as character states (especially those repre- tions of leaf cushion morphology, notably in cushion senting ornamentation) tend to replace each other complexity below Diapkoroden-dron-Synchysi in entirety rather than accumulating as sequential dendron, and in overall shape below Lepidoden elaborations of form (i.e., they are displacive rather dron—LepLdophloios. In contrast, cushion and leaf, than additive). Consequently, patterns of increasing trace simplification is evident in Hixentodendron.. complexity cannot be expected. Indeed, many spore The analysis of vegetative characters only (Fig character states (including the more elaborate forms 11) places Hizemodendron much lower in the tree of ornamentation) are confined to the primitive, eliminating the many character losses shown in bisporanglate OTUs. Reduction to a single func- Figure 6 but depicting the leaf cushion per se as tional megaspore resulted in the loss of all types iterative in (a) Hizemodendroit and (b) all of the of dispersed ornamentation (Table 3), suggesting arboreous genera, shown clustered above Chalo- that they were redundant once megaspores had nerUi in Figure 11 (also, arbitrary optimization of ceased to be the basic units of dispersal. missing values representing the absence of coded Relatively little attention has been paid to the structures led to the nonsensical apparent evolution functional morphology of lycopsid spores. Promi- of specific leaf cushion features below Paiiroden.- nent equatorial {Paurodendron, Chalonerid) and dron, prior to the evolution of the cushions them- \^e&ura\{PaurQdendron., OxroadLa., Diapkorodan- selves). Further modifications of cushion shape, dron, Synchysideiidron.) megaspore ornamenta- together with the appearance of infrafoliar parich- tion has been invoked as an aid to Rotation and nos and a return to longitudinal protoxylem ridges, thereby dispersal. Phillips (1979) argued that open- characterize the highly derived Lepidodendron- ings in the massa of Diapkorod&ndron. and Syn- Lepidophloioi clade (Fig. 6), ckyiidendron megaspores trapped microspores to Stelar characters, together with peridermal fea- facilitate fertilization, and a similar function was tures, play important roles in the more derived attributed to the anastomosing fimbriate laesural portion of the arborescent lycopsid clade, partic- Volume 79, Number 3 Bateman et al. 541 1992 Arborescent Lycopsid Phylogeny

ularly in delimitrng the three main cushion-bearing emit leaf traces that are sheathed by parenchyma clades: SigilUiria, Diapkorodendroit-SynckysL- when passing through the outer cortex, a character dendron, and Hi^emodendron—Lepidodendron.- state also found in SigiUaria sp. nov. Leaf traces Lepidopkloios. The solid protosteles of Oxroadia are secretory in most of the arboreous species and Paiirodejidron give way to raeduJlation by analyzed. parenchymatous vitalization in the reraainitig gen- Periderm is arguably the most unusual and de- era. In most of these, the central portion of the velopmentally intriguing vegetative tissue in ar- stele consists of parenchyma cells that have lengths borescent lycopsids. As with stelar morphology, the and diameters similar to those of the innermost Diapkorodendron-Synckysidendron clade is dis- metaxylem tracheids; these appear to he procam- tinct from the other cushion-bearing arboreous gen- hial cells that remained unlignified. and thus met- era. Bifaciahty in the former group is evident in abolicaliy active throughout the hfe of the plant. the clear histological distinction between the thin In the largest axes of Lepidodendron. and Lepi- phellem and much thicker phelloderm. The rela- dapkloios (less L. harcourtii), the stelar core con- tively homogeneous periderm of the latter group sists of filamentous cells that probably proliferated may conceal cryptic cambial bifaciality (for ex- into a central void. In contrast with the other ample, this may be manifested in the peridermal lycopsid genera but in parallel with ferns, the Dia- trizonation of Lepidodendron-Lepidophloios), es- phorodendron-Synckysidendron clade evolved a pecially if the phellem is very weakly developed or true siphonostele. Pith parenchyma cells are much the phellem and phelloderm are histologically iden- shorter and narrower than the adjacent metaxylem tical. Details of periderm histology tend to be ho- tracheids, suggesting different developmental ori- moplastic or species-level autapomorphies, and gins for these tissues. Didphoyodendron. has a mixed therefore of limited phylo^enetic value. In the anal- pith of parenchyma and tracheids, with parenchy- ysis of vegetative characters only (Fig. 11), pro- ma increasing in relative abundance toward the motion of Sigillaria to sister group of the Lepi- centers of larger axes. Synckysidendron. has a pith dodendron-Lepidophloios clade united the three region sharply delineated from the tracheary cells, genera that possess resinous periderm. However, and wood with heterogeneous rays and deep pa- the other two characters supporting this node renchymatous in vagi nations. (cushions on twigs wider than long, leaves with Most characters of the stelar margin constitute lateral abaxial grooves) are almost certainly mis- genus-level autapomorphies, notably the distinctly coded as homologs shared by Sigtliaria and Lep- different modes of leaf trace emission observed in idadendron-Lepidapkloias. Ckalonena, SigUlaria, and Lepidophloios (Fig. Periderm, the main support tissue of the arbo- 5). Of greater interest is the apparent switch from reous lycopsids, reached thicknesses of at least 20 distinct longitudinal protoxyleni ridges {yielding cm in some species (DiMichele, 1979a, b, 1981; "coronate" cross sections) to no discernible ridges Phillips & DiMichele, 1981). This considerable immediately above the primitive Paurodendroa— increase in trunk girth over that of the primary Oxroadia clade, followed by a return to similar tissues is difficult to reconcile with the persistence (but not identical) coronate morphology in the moat of primary leaf cushions, which probably remained derived Lepidodendron-Lepidophloioi clade; the photosynthetic after leaf loss; they are covered in protoxylem ridges are further modified in Lepi- stomata (Thomas, 1970b, 1977; DiMichele, 1979a, dophloios, where they anastomose (Fig. 6). Deri- b), and both leaf traces and parichnos connections vation of Hizemodendron from Lepidodendron with leaf cushions were maintained through the (contra Fig. 12; see Heterochrony) would imply periderm (Delevoryas, 1957; DiMichele, 1980). loss of protoxylem ridges. We suggest that the loss Several specialized mechanisms for accommodat- of ridges does not reflect complete absence of dis- ing girth increase evolved: tangential interarea ex- crete protoxylem strands, even thoygh the strands pansion in Sigillaria and Synckysidendron, in- are no longer discernible. terarea Assuring in Diaphorodendron, and Cortical characters of the arborescent lycopsids subcushion cellular expansion in Lepidodendron are surprisingly conservative compared with the (DiMichele, 1981, 1983). In arboreous genera with other axial tissues. The persistent inner cortex may well-developed crowns (Synckysidendron, Lepi- have provided a barrier of live cells along the outer dodendron, Lepidopkloios), periderm thickness margin of the phloem, protecting this delicate tissue diminished through the branching systems and the from exposure to the central void created by the cortex was probably a major support tissue. presumed in vivo disintegration of the thin-walled Given the determinate growth of arborescent parenchyma of the middle cortex. The meduUated lycopsids (Andrews & Murdy, 1958; Eggert, 1961), steles of Dia.pfioroden.dron. and Synckysidendron, most of the periderm probably formed and differ- 542 Annals of the Missouri Botanical Garden

entiated near the stem apex, during {though prob- a scar immediately external to the ligule pit ap- ably continuing after) differejitiatioii of the primary erture, occurred within the leaf rather than at the cortex, leaf cushions, and traces. This coordinated leaf-axis junction. Moreover, there is no evidence developmeot Ls indicated by the persistence of the of a discrete abscission layer. Thus, we suspect vascular linkages between the stele and leaf cush- that leaf laminae merely withered and sheared off ions through the periderm, and the occurrence of at the physically weakest point, where the leaf arboreous genera lacking specialized cushion-re- constricts and is perforated by the ligule pit and, tention mechanisms (Anabathra, Lepidopklaios). in the more derived genera, by the foliar parichnos. This mode of growth implies a stem apex analogous Acute leaf posture is strongly homoplastic, char- to the primary thickening meristem of some mono- acterizing unrelated genera with relatively short, cotyledonous angiosperms, an assertion previously hroad laminae (Paurodendron, Anabathra, Chal- made for stigmarian apices (Rothwell & Pryor, oiteria, Hieemodendron). The derived arboreous 1990, 1991). Unfortunately, there have been few genera (above Ckaloneria) all possess leaves with discoveries of anatomically preserved stigmarian sclerenchymatous sheaths, which presumably sup- apices (RothweU, 1984; RothweU & Pryor, 1991) ported the long, narrow laminae. Interestingly, the and none of stem apices, despite detailed and pro- sheaths were lost in the short-leaved pseudoherb longed studies of coal balls. Their rarity may he Hizemodendron. (Fig. 6). Expansion and invagi- at least partly explained by preferential decay of nation of traces may also have aided structural the apex, as observed in Ox.ro

man, 1989; Bateraan & DLMichele, 1991). Bauplan (2), which corresponds to Schoute's Rhizomorph and stem are ubiquitous modules, architectural model, is the most widespread among though both occur in a severely reduced form in the OTUs. Stems divide acrotonously (distaUy) hy some OTUa. Lateral branches/cauline peduncles equal division of the apical meristem, yielding mod- and crown branches are each rare or absent from ular (determinate), orthotropic (three-dimensional) some OTUs, thus defining three basic hauplans: (1) branches. The bauplan encompasses two distinct neither type of branch present, (2) crown branching subgroups categorized by the arboreous and pseu- frequent, lateral branching generates peduncles doherbaceous habits respectively. only, and (3) crown branching infrequent, lateral The first subgroup includes the classic arboreous branching dominant. Variations in the sizes and genera Lepidodendron and Lepidophloios, to- secondary tissue contents of all four modules, and gether with Synchysidendroni^i^. 1). Throughout in the frequency of dichotomy of lateral and crown much of their life history, these trees consist of a branches, generate a range of growth habits (e.g., rhizomorph and telegraph polelike stem capped by HaUe & Oldeman, 1970; Halle et al., 1978; White, a massive primary body, undergoing frequent di- 1979; Tomlinson, 1982, 1983). We suspect that chotomous branching to form a determinate crown growth of the arborescent lycopsids in general, and only during the final phase of growth and subse- arboreous taxa in particular, was largely deter- quent monocarpic reproduction (DiMichele & Phil- ministic (genetically induced), offering much less lips, 1985). The cones were borne on stout pe- potential than angiosperms for opportunistic mod- duncles that we regard as the homologs of more ification of growth architecture by environmental elaborate lateral branches found in bauplan (3); influences or chance factors (e.g., Tomlinson, although evolutionarQy significant, the peduncles 1982). Consequently, the conceptual architectural do not define, the architecture of bauplan (2) trees. model was unusually faithfully reproduced in the These trees were cheaply constructed. Secondary actual habit (Bateman & DiMichele, 1991). thickening ceased well before termination of growth; The three basic bauplans outlined above broadly the resulting poor development of wood in both the correspond to three of the growth models reviewed crowns and the trunks meant that they relied pri- by Halle et al. (1978); two can be subdivided using marUy on periderm for structural support (Di- growth habit. Michele, 1979a, b, 1983; Wnuk, 1985). This Bauplan (1) corresponds to Corner's architec- probably allowed channeling of more photosynthate tural model. In our analysis, this exclusively mono- into reproduction. Rapid generation times and an axial growth is confined to Ckaloneria, though opportunistic life strategy were postulated for the several penecontemporaneous lycopsids apparently subgroup by DiMichele & Phillips (1935). possessed the same habit; these include Spencerites The second subgroup, consisting of Pau,roden- (Leisman & Stidd, 1967), SporangLostrohus dron, Oxroadia, and Hizemodendron, is delimited (Wagner & Spinner, 1976; R. H. Wagner, 1989), by the pseudoherbaceous growth habit (Bateman, Porostrobus (Leary & Mickle, 1989), and the as 1988, 1989, 1992; Bateman & DiMichele, 1991). yet unnamed, almost fully articulated compression These genera possess the same modules as Lepi- from the Upper Devonian Cleveland Shale of Ohio dodendron and Lepidophloios, but differ in the (Chitaley, 1932, 1988; S. Chitaley & K. B. Pigg, relative sizes and shapes of the modules (Fig. 2a, in prep.). Ckaloneria is the only OTU in our anal- c, d). Also, overall body size of mature individuals ysis that consists only of the two ubiquitous mod- is one to two orders of magnitude less than those ules, a rhizomorph and an unbrancbed stem (Pigg of comparable arboreous species (cf. Fig. 1 with & RothweU, 1983a). We have classified its re- Fig. 2). In particular, the ubiquitous modules of peated zones of cauline sporophylls as lateral rather rhizomorph and stem are greatly reduced (most than terminal fructifications, as their production drastically in Paurodendron) relative to the crown, did not necessarily result in cessation pf stem growth. which develops much earlier in the life histories of The wood cylinder is narrow and the stem erect these genera. Their minimal stems result in a re- but much shorter than those of the truly arboreous cumbent growth habit (Baxter, 1965; Schlanker OTUs (cf Fig. 2b with Fig. 2a-g). The low wood & Leisman, 1969; Bateman, 1988), though de- content and lack of branches and cones in Chal- velopmental constraints preclude adaptations typ- oneria demonstrate highly economical construc- ical of truly prostrate growth (Bateman & Di- tion, implying rapid growth. Distributional evidence Michele, 1991). Nonetheless, these plants suggests that Cha.lon.eria was an ecological dom- superficially resemble the hasally branched archi- inant in marshlike associations (DiMichele et al., tectural model of Tomlinson (HaQe et al., 1978). 1979). Restriction of wood to the rhizomorph and highly 544 Annals of the Missouri Botanical Garden

reduced stem defines the pseudoherbaceous habit termine the ecological niches of specific arboreous sensu Bateraaji (1988), Rapid determinate growth lycopsids, a hypothesis that can be broadened to and a strongly r-selected life strategy are ioferred encompass nonarboreous arborescent species for these species, though whether their reproduc- (Bateman, 1988; Bateman & DiMichele, 1991). tion was extended, or monocarpic upon, cessation Bateman & DiMichele (1991) further suggested of growth, remains equivocal (Bateman, 1988; that transitions in many of the characters describ- Bateman & DiMichele, 1991). ing more detailed aspects of vegetative morphology Bauplan (3) also encompasses two subgroups. It reflect evolutionary changes in growth architec- characterizes Anahathra, Diaphorodendron sens, ture. If so, it is especially important to assess the str., and Slgillarla, as well as the reconstructed frequency and polarity of architectural changes adpression Bothrodendrait punctatam {Wnuk, during the history of the arborescent lycopsids. 1989). All share Stone's architectural model and Our character analysis (Table 3) focused on the arboreous growth habit. Stone's model resem- specific homologous structures, whereas the five bles Schoute's model in many parameters but ex- growth habits outlined above are polythetic sum- hibits clear differentiation between stem and lateral maries of several individual character states, some branches, which were produced throughout much apomorphic and some plesiomorphic (C1-C7). For of the life of the individual. Although a degree of example, the arboreous habit corresponds with the dorsiventral flattening has been inferred for the apomorphic state of Cl, the pseudoherbaceous habit lateral branches (Wnuk, 1985), their stable mor- with the plesiomorphic state of C2, and the pe- phology and spiral phyUotaxy suggest persistent dunculate habit with the plesiomorphic state of C7; orthotropy sens. lat. rather than a transition to Schoute's model with the apomorphic state of C3, plagiotropy (cf. Halle et al., 1978, table 7). De- Stone's model with the apomorphic state of C6, viation from Stone's model occurs during the final and Comer's model with the apomorphic state of phase of determinate growth, occasional isotomous C5. Despite their heterogeneity and partial depen- divisions (Hirmer, 1927; DiMichele & Phillips, dence on the cladistic characters, there is consid- 1985; Wnuk, 1985), presumably heralding ex- erable interpretative value in mapping the distri- haustion of the apical raeristem. However, the ef- butions of the growth habits across the preferred fect of such divisions is much less profound in MPTs. The procedure is not wholly tautologoua, bauplan (3) than in bauplan (2). Our assignment as the preferred MPT for analysis B (habit char- of Sigillaria to Stone's model, which contradicts acters omitted) is identical to that for the complete HaQe et al.'s (1978, fig. 71) assertion that the analysis (A; Fig. 9a), suggesting that habit char- genus conforms to Schoute's model, reflects our acters had little direct effect on the topology of the view that the stout cauline peduncles of Sigillaria latter. (and the bauplan (2) genera) are homologous with Two of the five growth habits (Corner's model entire lateral cone-bearing branches ai Anahatkra in Ckaloneria, pedunculate Stone's model in Sig- and Diaphorodendron; thus, by definition, Sigii- illaria) are autapomorphic at the generic level, laria possesses lateral branches, though we distin- preventing assessment of their phylogenetic sig- guish it as a separate architectural subgroup. nificance. The preferred MPT for analysis A (Fig. This group of polycarpic plants possessed ex- 6) requires homoplasy wi at least two of the re- current trunks and deciduous lateral branches. Wide maining three growth habits (pseudoherbaceous cylinders of wood and periderm occur in the trunks Schoute, arboreous Schoute, lateraUy branched of all the members of the group; they extend into Stone). It is equaUy parsimonious to assume a pseu- the lateral branches of D. scleroticttm, suggesting doherbaceous or arboreous hypothetical ancestor. greater persistence (DiMichele, 1980, 1981, 1985), In the first case, pseudoherbaceousness is replaced Growth and reproduction were both prolonged and by arboreousness immediately below Anabathra, sustained, conferring greater tolerance to extrinsic with a reversal to pseudoherbaceousness in Hize- stress and allowing these species to occupy suitable modendron. The transition to Stone's model also habitats for considerable periods (DiMichele & occurs immediately below Anabathra, with re- Phillips, 1985; DiMichele et al., 1987). Relatively sumption of Schoute's model in Diaphorodendron, sporadic reproduction and apomixis (presumably and the Hizemodendron—LepiAodendron—Lepi- facultative) have been reported in Sigillaria ap- dophloios clade. The only sister groups that un- proximata (Schopf, 1941; Phillips, 1979; Di- equivocally possess the same habit are Paaroden- Michele & PhiUips, 1985). drort and Oxroadia at the base of the.cladogram DiMichele & Phillips (1985) argued that growth and Lepidodendron and Lepidophloios at the apex. architecture and mode of reproduction largely de- Moreover, there is no clear evolutionary trend Volume 79 Number 3 Bateman et al. 545 1992 Arborescent Lycopsid Phytogeny

throLLgh the cladej Schoute's model characterizes modendron became pseudoherbaceous by hetero- both the most primitive and most derived genera. chronic reduction from an arboreous ancestor. Pre- We expected analysis D, baaed only on vege- cocious division of the primary apical meriatem tative characters, to provide a less homoplastic minimized the length of the stem and prompted distrihution of the major vegetative architectures. many subsequent character changes to accom- The most profound difference is the unification of modate the new growth habit. Reduction in size the pseudoherbs (aQ attributed to Schoute's model) and change in shape of the stem of Hlzemodendron. as a basal paraphyletic group, thus depicting Hize- imply progenesis, a form of paedomorphosis (re- modendron as much more primitive than it appears tention of ancestral characters in the descendant in the full analysis (cf. Fig. H with Fig. 6). The adult). topology for Figure 11, unlike that for Figure 6, In this paper, we are concerned less with the requires recognition of the pseudoherbaceous hahit details of the postulated mechanism of vegetative asplesiomorphic. Although .^n.a6*(/ir

ing biaporangiate-coaed genera (Chaloneria and well-supported conclusion from our study is that Anahatkra) m Figure 12. As in the case of Hize- Chaloneria is more primitive than the most prim- modendron, their primitiveness relative to OTUs itive member of the clade delimited by reduction witJi similar reproductive morphology is determined to a single functional megaapore per megasporan- by vegetative characters. Anabatkra is the orily gium (i.e., than Diaphorodendron-Synchysiden- bisporangiate-coned tree included in our analysis dron). and therefore provides the only potential arboreous The phylogenetic position of Chaloneria is es- ancestor for Oxroadia and Paarodendron. How- pecially significant because it is the oldest recon- ever, the three OTUs differ in many spore char- structed genus currently assigned to the Isoetales acters, and the unbranched rhizomorph and su- (Pigg & RothweU, 1983a; RothweQ & Erwin, 1984). perficial ligules of Paurodendron, label the genus A sister-group relationship with a widely recognized as relatively primitive or relatively derived, de- lepidodendralean genus such as Sigillaria (e.g.. pending upon near-arbitrary polarization decisions. Fig. 9k) would imply paraphyly of the Lepidoden- Other bisporangiate-coned trees, once reconstruct- drales and support Meyen's {1987: 70-81) deci- ed, wiU provide more credible ancestors. sion to synonymize the Lepidodendrales into the A heterochronic origin for Oxroadia and Paur Isoetales. Further resolution of these problems re- Todendron would weaken our analysis, as an a quires a broader cladistic analysis that includes priori assumption of their primitiveness was used other bona fide isoetaleans (including Isoetes), po- to polarize most of the characters (i.e., they were tential arboreous ancestors (e.g., Lepidodendrop- used as partial outgroups). Inclusion in the data sis-Protostigmaria: Jennings, 1975; Jennings et matrix of even more primitive OTUs may support al, 1983), and ostensibly more primitive OTUs our original assumption that Paurodendron and (e.g., SelagineUa) (see Bateman, 1992). Oxroadia are sister groups to the remainder of the arborescent lycopsid clade.- Our concern is largely Outgroups and ancestors Thus, we return to the driven by our opinion that the first arborescent fundamental questioris that prompted this study. lycopsid would have generated secondary tissues What character states delimit the Lepidoden- throughout its bauplan (the most simple develop- drales? Is the group monophyletic? If so, what is mental transition from inability to generate sec- the most appropriate outgroup? The chosen answer ondary tissues), and that restriction of wood to to this question leads to an even more loaded ques- certain modules reflects subsequent developmental tion: What is the most probable ancestor of the modifications. Moreover, determinate growth and ingroup? It also largely determines perception of a centralized rhizomorphic rootstock are characters the phylogenetic relationships among the ingroup shared hy aQ the OTUs, suggesting that they have members. exceptionally high burden (i.e., they play pivotal We believe that the greatest weakness of our roles in the development and function of the or- analysis is the narrow temporal and ecological range ganism and influence other dependent characters: represented by our OTUs; most of the species are Riedl, 1979; Fortey & Jefferies, 1982; Donoghue, restricted to at most the ca. 10 Ma of the West- 1939). These high-burden characters represent se- phalian(Fig. 3) and to the coal swamps of Euramer- rious ontogenetic constraints to a truly prostrate ica. However, the main phylogenetic groups within growth habit (Bateman & DiMichele, 1991), and the Lepidodendrales (or at least species possessing the bauplan appears much better adapted to up- many of their diagnostic character states; whole- right growth. Increase in body size to arboreous plant reconstructions have not yet been achieved proportions may have occurred subsequently rath- for pre-Westphalian arboreous lycopsids) can be er than concomitantly with acquisition of wood. traced back at least another 20 Ma, to the Ashian. Although Chaloneria is not a pseudoberb and Moreover, reproductive organs consistent with the is erect, the cladograms for all characters (Fig. 6) most apomorphic genus, Lepidophloios, have been and vegetative characters only (Fig. 11) show that recovered from Ivorian strata, a fur.ther 15 Ma its unbranched, bilaterally symmetrical rhizome, older (Fig. 3, inset; Long, 1968). This implies that unbranched stem, and cauline sporophyUs (all aut- all of the sister groups of this genus had diverged apomorphies in our analysis) are derived. This con- by the Ivorian; unfortunately, only one of our OTUs clusion is tempered by the possibility that Chalo- (Oxroadia gracilis^Oxroadia sp. nov.) was re- neria is not a genuine member of the ingroup, constructed from such early assemblages. As yet which would explain its numerous autapomorphies incompletely reconstructed arboreous lycopsids (not and its role as the greatest cause of topological necessarily bona fide lepidodendraleans) were wide- instability in each analysis (Figs. 9, 10). The only spread and at least locally ecologically dominant Volume 79, Number 3 Bateman et al. 547 1992 Arborescent Lycopsid Phylogeny

by the latest Devonian (e.g., Scheckler, 1986a, b; session of rootlet-bearing rhizomorphs, secondary DiMichele et al., 1992). tissues (wood and periderm), ligules, and hetero- Thus, the combination of the stratigraphic rec- spory (Chaloner, 1967; Stewart, 1983). These ord and our phylogeny suggests that the three main structures provided the holapomorphies that unite groups of monosporangiate-coned genera recog- aU the OTUs included in our analysis (Fig. 6), but nized in our cladistic analysis (Sig'dlaria, Diapho- most (possibly all) have a greater level of univer- rodendronSynckysidendron, Hizemodendron- sality. For example, a wide range of enigmatic latest Lepidodendron-Leptdophloios) diverged at least Devonian and earliest Mississippian lycopsids pos- 35 Ma prior to the Westphalian coal-swamp lager- sessed wood (Meyer-Berthaud, 1981, 1984; statten that provided most of our OTUs. This would Scheckler, 1986a, b; Matten, 1989; Roy & Mat- explain why these groups show similarly large de- ten, 1989). Rhizomorph-like, rootstocks, ligules, grees of divergence from their putative bisporan- and heterospory aU characterize homophyUous Se- giate-coned ancestor(s) (Fig. 14) and are supported laginella, the type genus of theSelagjneUales(e.g., by many character-state transitions (Fig. 6). Al- Bierhorst, 1971; Bold et al., 1980). Moreover, ternatively, the saltational evolutionary scenario Paurodendron (and therefore, by implication, its erected for major vegetative changes may be ex- sister genus Oxroadia) was assigned by Schlanker tended to encompass reproductive innovations, & Lejsman (1969) to SelagLnellA, and it is widely eliminating the need for intermediate taxa during accepted as a member of the SelagineUales (e.g., the early radiation of the group. Taylor, 1981; Stewart, 1983; Meyen, 1987). On Current evidence suggests that our morpholog- these criteria, the Lepidodendrales could be cir- ically divergent OTUs together exhibit most of the cumscribed to include both Paurodendron and character states possessed by the arborescent ly- homophyUous SeUtgineUa. copsids as a whole, including other Pennsylvanian Moving progressively up the clade, the next species and their Mississippian and Devonian an- OTU encountered is the most primitive tree, An- tecedents. However, the paucity of genera in our abathra. Regarding this OTU as the most primitive analysis, and the fact that most represent only the lepidodendralean would allow delimitation of the final period of the history of the group, invpUes that order using the arboreous habit and associated we have sampled only a restricted range of the modifications of stelar anatomy, together with foliar combiiKLtions of character states that existed. This parichnos. Unfortunately, many of these character would explain the large number of character states states are homoplastic as a result of loss during the that occur as genus-level autapomorphies in our hypothesized progenetic evolution of pseudoherbs cladogram (Fig. 6), leaving few character states to from trees: Hizemodendron from a Lepidoden- support the consequently weak links that constitute dron-like ancestor, and possibly Oxroadia and/or the main axis of the cladogram and determine Paurodendron from Anabatkra-like ancestor(s). perceived genus-level relationships. Inclusion of Although phylogenetically valuable, these char- older OTUs, dating back to the main radiation of acter states are not ubiquitous within the clade. the group, would probably alleviate this problem Many workers would argue that the clade is dehm- by transforming genus-level autapomorphies into ited primarily by possession of a stigra^rian rhi- genus-level synapora.orphies. In an alternative less zomorph. However, we were unable to identify any gradualistic scenario, the large number of genus- profound characters that distinguish the stigmarian level autapomorphies may reflect evolutionary dy- rhizomorph of Anabatkra from the supposedly namics, particularly the simultaneous origin of nonstigmarian rhizomorph of Oxroadia, which is blocks of characters linked by pleiotropic or epi- much smaller and more compact but otherwise very genetic factors (e.g., Levinton, 1988). This mode similar. Also, this clade contains Chaloneria, an- of evolution may be difficult to resolve cladistically other nonarboreous OTU. Chaloneria possesses for a variety of methodological reasons (these will several autapomorphies, notably an unbranched be discussed in a future paper; see also Lemen & stem lacking cones and a bilaterally symmetrical Freeman, 1989). rhizomorph, that suggest affinities with the extant Older OTUs are also needed to determine con- genus hoetes. If Pigg & Rothwell (19S3a) cor- vincingly whether the Lepidodendrales are mono- rectly ascribed Chaloneria to the Isoetales, and if phyletic and in particular to provide more satis- the genus is correctly positioned in our phylogeny factory outgroups. However, before these questions (which is by no means certain; Fig. 9), inclusion can be addressed, the character states that sup- of Anabathra in the Lepidodendrales -and contin- posedly delimit the Lepidodendrales should be re- ued recognition of the Isoetales would render the viewed. Four are most commordy cited: the pos- former order paraphyletic (Appendix lA). 548 Annals of the Missouri Botanical Garden

Perhaps the most cohesive clade includes Sig- phorodendron-Synchysidendron,), and Lepido- illaria as its most primitive genus. It is delimited dendraceae (LepidopkloLos-Lepidodendron- by the nonhomoplastic synapomorphies of leaf Hisemodendron.). Each family is supported by sev- cushions and monosporangiate cones that generate eral character state transitions (Fig. 6). megasporangium-megasporophyU disseminules. We Evidence for the postulated monophyly of the are confident of the monophyly of the three main monosporangiate-coned clade, and for the primi- groups of OTUa that constitute the clade (Sigil- tiveness of the 5igiUariaceae relative to the Dia- iaria, Diaphorodendron-Synchysidendron, Hi- phorodendraceae and Lepidodendraceae, is more zemodeTidroih—LepiAodendron—Lepidopkloios), equivocal. This largely reflects our inabUity to make and our parsimony analysis strongly supports confident statements concerning phylogenetic re- monophyly of the clade as a whole (nevertheless, lationships among the four primitive, biaporangiate- we note that such an adaptively valuable suite of coned genera. They form a highly heterogeneous, character states could reflect parallel responses in paraphyletic (or possibly polyphyletic) plexus of two or more lineages to similar selective regimes, disparate morphologies that share a free-sporing thus confounding parsimony: cf. Coddington, 19S8). mode of reproduction. Oxroadia and Patiroden- Given that our assumption of homology among the dron differ in many characters and are united in three lineages in monosporangiate cones and the Figure 6 by arguably only one synapomorphy; we megaaporangium-megasporophyll complex as dis- doubt their apparent monophyletic status. Only sera-inule is the crux of the preferred MPT (Fig. Anahathra is a tree; the paeudoherba Oxroadia 6), these characters merit even more careful scru- and Pau.roden.drQn and possibly even the shrub- tiny. For now, we refer to this clade, more narrowly sized phallos ChaUmeria are potential progenetic defined than moat perceptions of the Lepidoden- descendants of trees broadly similar to, but prob- drales, as the "Segregationists" (referring to the ably distinct from, Anabathra. segregation of megasporangia and microsporangia Determining the origin(a) of the monosporan- in different cones). Members of the less inclusive giate-coned clade wdl require inclusion of pre- clade that excludes Sigillaria and is deUmited pri- Pennsylvanian monosporangiate-coned species and marily by reduction to a single functional mega- a broader selection of bisporangiate-coned trees; spore that germinates within the sporangium are several potential candidates, aQ requiring further the "Isolationists." reconstruction before they can be used with confidence in cladistic analyses, are listed in Table 5. Determining the origin(s) of the arboreous lycop- CONCLUSIONS sids, and of putatively progenetic bisporangiate- Empirical observations. We are confident that coned genera such as Oxroadia and Pauroden- each of the 10 genera analyzed by us is mono- dron, also necessitates inclusion of more distantly phyletic. This conclusion is not especially profound, related nonarborescent lycopsids (e.g., Selagiaella as six of the genera are here represented by only sens, lat., Leclercqia] to reassess character state one species and thus not cladistically testable (Fig. polarities. Given these observations, we envisage 8). The analysis prompted segregation of two new eventual redelimitation, or possibly amalgamation, genera: Hizemodendron from Lepidodendron of three widely recognized lycopsid orders (Appen- (Bateman & DiMichele, 1991), and Synckysiden- dix lA; see also Bateman, 1992). drojh from Diaphoroderidron (DiMichele & Bate- Absence from the present analysis of nonarbo- man, 1992). However, these decisions were taken rescent species and of any credible ancestor of the primarQy on the grounds of differences in several most primitive arboreous genus (Anabathra) to- characters (many directly or indirectly reflecting gether prevent determination of whether arbores- different growth architectures) rather than as at- cence (secondary thickening) and arboreousness tempts to disaggregate para- or polyphyletic groups. (large body and upright growth) evolved simulta- Diapkorodendron-Synchysidendron, is undoubt- neously or sequentially. Other especially important edly monophyletic; Hizemodendron-Lepidoden- and potentially linked innovations that possess a dron is depicted in Figure 6 as paraphyletic but, higher level of universality than our ingroup are as we have argued, may nonetheless be monophy- determinate growth and the centralized rhizo- letic. Derived (monosporangiate-coned) genera morphic rootstock. In general, the most significant constitute three distinct monophyletic clades that evolutionary advances within the bisporangiate- are most appropriately regarded as families: Sig- coned plexus appear to have involved- vegetative illariaceae (Sigillaria), Diaphorodendraceae (Dia- rather than reproductive organs, indicating that Volume 79, Number 3 Bateman et al. 549 1992 Arborescent Lycopsid Phylogeny

TABLE 5. Selected genera that are potentially phylogcnctically Informative but are currently insufficiently known to provide satisfactory cladistic data sets (listed in order of appearance in the stratigraphic record). We note that ^Lepidodendron* cai^ntopsold^s is not closely related to Lepuiadendron. sens, str- (R. M. Bateman, unptihliahed ohs.) and that Bolkrodendron sens. lat. is probably a polyphyletic aggregate of several disparate species (Scott, 1920; Thomas & Meyen, 1984). See also reviews by Chaloner (1967), Meyer-Berthaud (1981, 1984), and Nfatten (1989).

Lepidosigillaria wkitei Krausel & Weyland White (1907); Arnold (1947); Grierson & Banks (1963) [Late Givetian-Early Famennian: New York State] Protolepidodendropsls spp. Gothao & Zimmermann Haeg (1942); Schweitzer (1965) [Famennian: Euramerica] Trabu:a.alis spp. Meyer-Berthaud Meyer-Berthaud (1981, 1984); Roy & IVIatten (1989) [Famennian-Early Tournaisian: south-eentral Frartce; New York State) Cyclostigma kiitorkense Haugkton Johnson (1913); Chaloner (1967, 1968, 1984); Chaloner & Meyer-Berthaud (1983) [Struniant southwestern Ireland] Land^yrodendron spp. Meyer-Berthaud Meyer-Berthaud (1931, 1984) [Early Tournaisian; south-central France] Lepidodendropsis spp. Lutz-ProtostigmarLa eggertiana Jennings Lutz (1933); lurina & Lennoigne (1975); Jennmgs (1975); Jennings et al. (1983) [Tournaisian: Euramerica] Valmeyerodendron trmngularifotium Jennings Jennings (1972) [?Tournaisian; Illinois] Botkrod^ndron spp. Lindley & Huttoo Scott (1908); Weiss (1908); Calder (1933b); Stubblefield & Rothwell (1981); Wnuk (1989) [Tournaisian-Westphalian: Euramerica] 'LepidodsndrotJL {'iAna.bat.kTa) calamopsoides Long Long (1964, 1971, 1986); Scott & Galtier (1938) [Late Tournaisian: northern Britain] Leiiicaulis a.rTO.ne.nsis Beck Beck (1953); Pant & Walton (1961) [Mid-Visean: southwestern Scotland] 'Lepidodendron (lPhytokrMm.e) hrownii Unger Chodat (1911); Calder (1933a); Meyer-Berthaud (1981) [Visean; southern Scotland]

they are economic adaptations (sensu Eldredge, dendraceae and Lepidodendraceae (Fig. 3). Such 1989) employed continuously in competition for extinctions of major monophyletic groups are un- resourcea. The cladograms imply that the well- common (Smith & Patterson, 19SS) and require documented sequence of reproductive innovations a causal rather than a purely stochastic explana- in the monosporangiate-coned clade, which ulti- tion. mately led to seed analogs in Lepidophlaios (e.g., These analyses provide useful (if circumstantial) Phillips, 1979), occurred later, though they may evidence for the relative burden of particular types have been developmentaUy Unkedto additional veg- of character, in the guiae of amounts of homoplasy. etative modifications (this hypothesis requires fur- Interestingly, this partly reflects the physical scale ther study). Interestingly, the equally weU-docu- (dvmensions)of the feature represented hy the char- mented, clitnatically driven end-Westphalian acter relative to that of the plant body. Characters extinctions of specific elements of the coal-swamp of Largest scale (notably overall growth hahit) and floras (PhiUips et al., 1977, 1985; Phillips & Pep- smallest scale (e.g., various details of cellular his- pers, 1984) most seriously affected the most de- tology and spore ornamentation) are generally more rived portion of the arborescent lycopsid clade, homoplastic than those of intermediate scale, such eliminating the "Isolationist" families Diaphoro- as stelar and associated trace morphology, the basic 550 Annals of the Missouri Botanical Garden

structure of leaf bases and. sporophylls, and the tralized rhizomorphic rootstock, together with the nature of the dispersal unit. As a broad general- small number of module types that constitute the ization, large- and small-scale features delimit spe- bauplan, predisposed the plants to profound het- cies and genera, intermediate scale features delimit erochronic changes in body size and body plan; we families or still higher taxa. believe that these were manifested as geologically The results of our study will not encourage pro- instantaneous events resulting from changes in de- ponents of organ phylogenies. Merely bisecting our velopmental regulation. This saltational evolution- data matrix into submatrices representing vege- ary scenario has considerable predictive value, par- tative (Fig. 11) and reproductive (Fig. 12) organs ticularly if considered in tandem with advances in generated substantially different preferred MPTs understanding of the ontogeny, functional mor- that were clearly inferior to the preferred MPT of phology and physiology of these remarkable or- the fuU matrix (Fig. 6). The analysis of reproductive ganisms (e.g., PhUlips & DiMichele, 1992). More- organs could not satisfactorQy resolve the relation- over, saltational scenarios can be falsified (or at ships among the four most primitive and three most least highly modified) hy cladograms, if the pre- derived genera. The analysis of vegetative organs dicted positively correlated suite of character state misplaced Hizemodendroa as unduly primitive and transitions is dissociated (e.g., hy the interpolation Sigillaria, as unduly derived and could only dis- of additional OTUs onto the internode in question: tinguish Synchysidendroa from Diapkaroden- R. M. Bateman, in prep.). dron using cone axis characters that mirror those We have been unable to discern any substantive of ultimate vegetative axes. Nonetheless, the ar- differences between reconstructing the morpholog- boreous members of the three niiiust derived famdies ical phylogenies of extinct and extant species (cf. (Sigillariaceae, Diaphorodendtaceae, Lepidoden- Stein, 1987; Gauthier et al., 1988; Donoghue et draceae) persist as clades in the analyses of both al., 1989; Boy, 1990). The inevitable typological suhmatrices. This shows that the families as cur- nature of conceptual whole-plant fossils is not det- rently known can be approximately delimited using rimental in the essentially typological realm of cla- either vegetative or reproductive characters alone, distics. Our 16 OTUs undoubtedly represent a even if their relationships cannot be determined highly rarified sample of all the arboreous lycopsid accurately. species that ever existed. This contributed to sev- Our results are even less encouraging for clas- eral problems, notably the broad morphological sifications based on even more reduced suites of discontinuities separating some cladeff(Fig. 14) and characters. We have identified homoplasy in many the absence of satisfactory outgroups. However, supposedly diagnostic character states, including cladistic analyses based exclusively on extant spe- some of the leaf-base detads that are traditionally cies are even more selective; unique character com- used to classify adpressed lycopsid axes. On the binations found only in the fossil record, especially basis of these observations, we support in principle during the initial radiation of a major clade, are the hierarchical system of well-known core taxa deliberately excluded. Similarly, opportunities to and less weU-known satellite taxa proposed for the use stratigraphie-temporal evidence to assist po- Lycopsida by Thomas & Brack-Hanes (1984), but larization and characters, and (more importantly) are convinced that reconstructed, anatomically to select among alternative topologies generated preserved whole plants provide better core taxa from the same data matrix, are squandered. The than the reproductive organs favored by Thomas question of excluding fossUs does not arise in the & Brack'Hanes. Certainly, whole-plant reconstruc- case of the monosporangiate-coned lycopsid clade, tions are essential prerequisites for convincing phy- which apparently lacks extant descendants. Despite logenetic and ecomorphic interpretations. the serious problems posed by incomplete preservation in the fossil record, we were able to score Methodological observations. We do not regard a large number of characters representing all or- phylogenetic reconstruction as, an isolated, objec- gans of our OTUs and generated a large data tive procedure divorced from hypotheses of evo- matrix containing only a smaQ proportion of missing lutionary mechanisms; rather, it is positive feed- values. Although technically feasible, inclusion of back between the two sets of paradigms that leads less weU-known, partiaQy reconstructed OTUs to greater understanding. The evolutionary history should be postponed pending further investigation of the arborescent lycopsids is not a simple story of the effects of missing values on tree-length cal- of progressively increasing complexity expressed culation and character state optimization. throughout the bauplan. In particular, high-burden This study indicates that well-understood fossds characters such as determinate growth and a cen- are as valuable for phylogenetic studies as any Volume 79, Number 3 Bateman et al. 551 1992 Arborescent Lycopsid Phytogeny

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FUNK. 1991. The Compleat Cladiat: A Primer of drales (secondary thickening, periderm, ligules, hetero- Phylogenetic Procedures. Univ. Kansas Mus. Nat. spory) is confined to the order. The present analysis shows Hist. Spec. Publ. 19. that the Lepidodendrales as currently delimited may not WELLARD, D. A. 19a9a. Source plants for Carboniferous be monophyletic, and even if monophyletic may not be microapores: Lycospora from permineralized Lepi- the most meaningful clade to use as the basis of an ordinal dostrobas. Amer. J. Bot. 76; 820-827. level classification (see also Matten, 1989). Together with . 1989b. Lycotpara from Carboniferous Lep- the Isoetales and Selaginellales, the Lepidodendrales re- idoitrohiis corapreasions. Amer. J. Bot. 76: 1429- quire redelimitation or amalgamation. 1440. B. Anabathra versus PaTalycopodit&i. We accept Pear- WILLIAMSON, W. C. 1372. On the organisation of the son's (1986) arguments that ParalycopadUes brevi/olms fossil plants of the Coal Measitrea, III. Lycopodiaceae (Williamson) DiMichele (formerly ^Lepidodendron'' brevi- (continued). Philoa. Trans. 162: 283-313. folium Williamson) is identical to, and a junior synonym . 1893. On tbe organisation of the fossil plants of, Anabathra palckeTrima Witham (cf. Witham, 1833; of the Coal Measures, XIX. Philos. Trans. 184: 1- Williamson, 1872), We also recognize that the adpression 38. genus Uladendron Lindley & Hutton (1831) both resem- WEMSATT, W. C. & I. C. SCHANK. 1988. Two con- bles and nomenclaturally pre-dates Anabathriit but sus- straints on the evolution of complex adaptations, and pect that Ulod^ndran is considerably more inclusive (i.e., the means for their avoidance. Pp. 231-273 Ln M. more broadly delimited) than Anabatkra- H. Nitecki (editor), Evolutionary Progress. Chicago Unfortunately, A. pulcherTuna is a form-species (sensu Univ. Press, Chicago. Bateman & Rothwell, 1990), having been correlated with WINSTON, R. B. 1988. Paleoecology of Middle Penn- several cone-species of the plesiomorphic bisporangiate sylvanian-age peat-swamp plants in Herrin Coal, Ken- genus Flemingites (DiMichele, 1930; Pearson, 1986). tucky, U.S.A. Int. J. Coal Geol. 10: 203-238. The type material of A. pidckerrima., from the Late WETHAM, H. T. M. 1833. Tbe Internal Structure of Tournaisian of AUanbank, southeastern Scotland, co-oc- Fossil Vegetables found in the Carboniferous and curred with La^gerdctila horrida megaspores (these were Oolitic Deposits of Great Brit^fin. Edinburgh. incorrectly referred to L. stibpdo^a by Pearson, 1986: WNUK, C 1985. The ontogeny and paleoecology of K. M. Bartram, pers. comm. 1987; H. L. Pearson, pers. L&pidodendron rimi)sij.m. and Lepidadendron bre- comm. 1987), which have been found in Flemmgites tonettse trees from the Middle Pennsylvanian of the graciiis cones (Chaloner, 1953; Brack-Hanes & Thomas, Bernice Basin (Sullivan County, Pennslvania). Pa- 1983). Elsewhere, A. puUherrlma co-occuia withF. 3cMtii laeontographica B 195: 153-181. at the Late Visean locality of Pettycur, southeastern Scot- . 1989. Ontogeny and paleoecology of the Mid- land (e.g., Williamson, 1872; Jongmans, 1930; Di- dle Pennsylvanian arhorescent lycopod Botkroden- Michele, 1980; Scott et al., 1984; Pearson, 1986), and dron. punctatu-m,, Bbthrodendraceae (Western Mid- with either F. ditentii or F. sckopfii at many .West phalian dle Anthracite Field, Shamokin Quadrangle, coal-hall localities in Euramerica (DiMichele, 1980). The Pennsylvania). Amer. I. Bot. 76: 966-980. differences between these cone-species arfivsubtle and not ZALESSKY, M. D. 19-1,2. The anatomy of icjnJdopWoioj readily resolved cladistically. In particular, our scoring of laricinus Sternberg. Etudes Paleobot. 2. St. Peters- A. pidckeTrima focused on Pennsylvanian rather than herg Lett. Sci. 1: 1-13. Mississippian assemblages; F. diversiLs (Westphalian D: ZHANG, S.-Z., D.-S. YEH & L.-Z. BiAN. 1936. On seed Felix, 1954) and F. sckSpfii (Westphalian B: Brack, and polyphylesia of seed plants, Palaeont. Cathay. 3: 1970) differ primarily in the mean number of megaspores 311-316. per megasporangium and thus were not differentiated in our data matrix (Table 3, Fig. 3). We anticipate taxonomic revision of vegetative and APPENDIX 1. NOMENCLATURAL AND TAXONOMIC NOTES reproductive organs oi Anabathra as increased knowledge (particularly of Mississippian forms) allows further whole- A. Higher taxa. Bateraan (1990b) recommended the supra-ordinal classification of Knoll & Rothwell (1981) plant reconstructions; for example, 'LepidodendrorC and ordinal classification of Stewart (1933); together, calamopsoiAes Long (1964), -which co-occurs with stig- these classifications imply monophyly of the Division Tra- marian rootstocks, fiemirag'ites-like strobili and Lagenl- cheophyta and Class Lycopaida, but present a provisional, cilia, crassiaculeata megaspores (Scott & Meyer-Ber- egalitarian (grade) arrangement of six orders within the thaud, 1985; Scott & Galtier, 1983; Scott, 1990), may Lycopsida (Drepanophycales, Protolepidodendrales, Ly- be a species of Anabathra (cf. Table 2). Such plants will copodiales, Selaginellales, Lepidodendrales, Isoetales). Ac- form the basis of a new arborescent lycopsid family, the Anabathraceae. quisition of further phylogenetic information will require Te-delimitation of these orders and their rearrangement Cr Er^ctUi'n of ncui gensra and species. We have delib- into a more hierarchical classification (Bateman, 1990h, erately avoided formal reclassificaticn of the 17 whole- 1992; Hueber, 1992). Colloquial'(informal) names are plant species included in our study. Thus, the three new consistently rooted in their formal counterparts; thus, species (one each of Oxroadiaj Sigillaria^ and Syn- "lycopsid" is used for the Class Lycopaida and "lepidoden- ckysidendron) remain unnamed (but see Bateman, 1992; dralean" for the Order Lepidodendrales (Bateman, 1990b). DiMichele & Bateman, 1992). At present, the Lycopsida are perceived as being de- However, the results of this study encouraged us to limited by exarch protostele, scalariform metaxylem with restrict further the range of variation encompassed by Williamson fimbrils, vascularized "microphylls," and fo- Lspidodendron sens, str., a process that was begtm by liar/axillary eusporangia (e.g., Stewart, 1983). With the DiMichele (1981, 1983, 1985) when clarifying the de- possible exception of stigmarian rhizomorphs, none of the limiting parameters of Lepidodendron, Lepidophloios, characters traditionally used to delimit the Lepidoden- and DiapkoTodendron sens. lat. In order to transform Volume 79, Number 3 Bateman et al. 559 1992 Arborescent Lycopsid Phylogeny

Lepidodendron from an apparently paraphyletic (Fig. 6) sporangia te A. takhtajanii-typc, (2) megasporangiate A. to a monophyletic entity, we retained only the anatomi- udruis-type, and (3) microsporangiate A. udriEis-type (Ta- cally preserved equivalent (L. hickii) of the type species ble 2). Groups (2) and (3) are restricted to Diapkoro- (L. actile.a.tu.m) and erected *Lepidodendrofi* serratiLTn dendran^Synchyside.ndron\ cones of all three Duipho- as the type species of a new genus, Hlzemodendran rodcAidro^ species and both SyncAyjideAidro^i species can (Bateman & DiMichele, 1991). The two genera share only be distinguished by the medullated steles of the latter aimilar reproductive organs, hut differ in many vegetative despite major differences in growth architectiLre and veg. characters; at least most of these differences may reflect etative anatomy between the two genera (DiMichele, 1981) the imposition of radically different growth habits on a Group (1) cones characterize Hi2e.m0de.ndTon and Lep shared bauplan^ idodendron (DiMichele, 1983; Bateman & DiMichele Although our study strongly supports monophyly for 1991). We believe that megasporangiate A. ta.kkla.ia.nii DuLphorodsndron sens. lat. (i.e., sensu DiMichele, 1985; and A. varuis are sufficiently distinct to merit generic see Fig. 6), the precedent of generic distinction of species distinction (the latter would require a new organ-genus). sharing similar reproductive organs but exhibiting major Assignment of megasporangiate and microsporangiate A. differences in growth habit and ontogeny requires the udrius to different cone-genera would be more consistent recognition of the two most apomorphic species, 'Z).' with the systematic treatment of HizemodsTtdron, Lep- dicentriciin and 'Di/ipkorodendron' ap. nov., as a new idodendran, and Lepidopkloios cones in Table 2, though genns of arboreous lycopsid, Synchy-tiAendron. In con- Phillips (1979: 256, 259) presented several argiLments trast with the more plesiomorpbic Diaphorodendron (epit- against this option. omized by the type species, D. vasculare), S, dicentricam, and Synchysideadron sp. nov. lack lateral branches and APPENDIX 2. ANALYTICAL ADVANCES were probably monocarpic (DiMichele, 1981, 1985; Bate- man & DiMichele, 1991; DiMichele Si Bateman, 1992), Given the appropriate microcomputers and software, thus possessing the same hauplan, growth habit, and re- more elegant solutions are now available to some of the productive strategy as Lepidodendron sens. att. (Fig. 1). diffictilties that we encoiLntered -when performing these analyses in 1989. For example, the problem of storage D. Revision, of the cane-genera.- As, currently delimited, of only superficially different topologies, resulting from cone form-genera serve as shorthand for co-occurring polychotomies, has been solved in Version 3.0 of PAUP complexes of character states. A few cone-genera are (Swofford, 1991). There is much to commend an ana- assignable to single stem-genera (Table 2), notably Ma- lytical approach that entails initial parsimony analysis in zocarpon to SigiMaria{&.%,, Schopf, 1941; Feng & Roth- PAUP 3.0, subseqiLent comparison of MPTs with those well, 1989) and Lepidocarpon, to Lepidopkloios (Di- generated by using Hennig86 Version 1.6 (Farris, 1989), Michele, 1983). The microaporangiate gentis and printing of interesting topologies and character state Lepidostrohu,s characterizes Hlzemodendran., Lepido- distributions using MacClade Version 3.0 (Maddison & dendron, and Lepidophl^ios^ cone-species of each of Maddison, 1991). Estimation of degrees of support for these stem-genera can only be distingiLished by continuotis particular nodes using bootstrapping (Efron, 1932; Fel- quantitative characters and microspore morphology (e.g., senstein, 1985; Sanderson, 1989) is gaining in popularity, Wlllard, 19a9a). lii' contrast, Ackla.m.ydocarpon is a though there is no statistical substitute for detailed ex- greatly inflated form-geniLs (e.g., Leisraan & Phillips, 1979) amination of suboptimal-length topologies. encompassing three main morphological groups: (1) mega-