Plant Paleoecology and Evolutionary Inference: Two Examples from the Paleozoic William A

REVIEW OF PALAEOBOTANY AND PALYNOLOGY ELSEVIER Review of Palaeobotany and Palynology 90 (1996) 223-247

Plant paleoecology and evolutionary inference: two examples from the Paleozoic William A. DiMichele \ Richard M. Bateman ''•= ' Department of Paleobiology, NMNH Smithsonian Institution, Washington, DC 20560, USA ' Royal Botanic Garden, 20A Inverleith Row, Edinburgh, EH3 SLR, UK ' Royal Museum of Scotland, Chambers Street, Edinburgh, EHl IJF, UK Received 5 September 1994; revised and acx»pted 20 December 1994

Abstract

Paleobotany can contribute much to evolutionary scenario-building. Here, we use two case studies — the Devono- Carboniferous vascular plant radiation and the largely coeval evolution of heterosporous from homosporous life histories — to examine the interface between phylogeny and ecology. Our observations challenge some tenets of the neo-Darwinian orthodoxy, notably the assumed role of competition mediated selection as an active driving force, rather than a passive filter, of evolution. The Devono-Carboniferous class-level radiation of vascular plants was prompted by attainment of a complexity threshold and delimited the morphological envelope that enclosed an apparently fractal pattern of subsequent, lower level radiations. The contrast of low speciation rates with exceptionally high rates of phenotypic divergence in the Devonian suggests a non-adaptive "novelty" radiation, perhaps reflecting saltational evolution via "hopeful monsters". Successive lower level radiations were more constrained by the ecological hierarchy that resulted from progressive niche differentiation and saturation. This in turn reflected increased speciation rates, thereby completing a well defined negative feedback loop in the coevolution of phenotypic and ecological diflierentiation. Heterosporous Ufe histories evolved independently in at least ten lineages. Heterospory allows the sporophyte to impose, via diiferential development, a single fixed gender on each gametophyte prior to spore release. Although the resulting life history is less flexible than homospory, which on recent evidence includes a range of subtle and sophisticated strategies, it promotes the sporophyte as the primary target for selection. Gametophytes effectively perform the role of gametes and are released into the environment prior to fertilization, thus favoring aquatic- amphibious habitats resistant to occupation by homosporous pteridophytes; terrestrial heterospory requires apomixis. Although the profound iteration of heterospory implies a strong adaptive advantage, repeated gradual evolution via inferior intermediates exhibiting exosporous heterospory seems unlikely. Seed-plant success reflects economic efficiency and the subsequent evolution of effective poUination syndromes, rather than integumentation of the ovule. Major radiations of heterosporous Uneages and subsequently of seed- plants required pertiu-bation of pre-existing commxmities by extrinsic environmental changes rather than genuinely competitive displacement. This typical manifestation of "home-field advantage" further emphasizes the intimate relationship between phylogeny and ecology, and allows us to make predictions that can be tested by further paleobotanical research.

1. Introduction the same time the breadth of morphological hypotheses has been enriched by modem concepts 1.1. Neo-Darwinism in paleobiology imported from developmental biology (Rothwell, 1987; Trivett and Rothwell, 1988; Mosbmgger, Fossils of vascular land plants reveal a record 1990; Stein, 1993; Bateman, 1994; Bateman and of vast morphological change and enormous taxic DiMichele, 1994a). Results include greater empha- diversification following humble beginnings in the sis on macroevolution (Wight, 1987; DiMichele Silurian. Historically, paleobotanists have applied et al, 1989; Bateman, 1994; Bateman and and extrapolated the tenets of neo-Darwinian DiMichele, 1994b), challenges to the concept of graduaUsm to explain the increase in plant struc- competition as the all-pervasive driving mechanism tural complexity. The focus has been on morpho- in plant evolution (Scott and Galtier, 1985; logical transformation, considered in isolation DiMichele et al, 1987; Valentine et al., 1991), and from the environment and often described in terms the recognition that selection may act more often of individual organs rather than in a whole-plant as a passive filter than as an active vector of context. Most theorizing has been limited to appli- evolution (Rothwell, 1987). cation of the axioms of gradual change to cases of These great strides have been made in a relatively presiuned ancestor-descendant relationship, often few years, yet one major aspect of a complete in progressive linear sequences of several taxa (e.g. picture remains poorly understood ecology (more Magdefrau, 1956). With a few notable exceptions specifically, the particular habitat preferences and (e.g. Stidd, 1980), the phylogenies themselves are limited ecological ampUtudes of each species). usually determined intuitively from the very same Commonly, ecology is assumed to influence evo- expectations of gradual descent with modification. lution through competition (e.g. Knoll, 1986), As a consequence, the literature is filled with though assertions about competition rely on the nimierous examples of hypothetical intermediates, usually untested assumption that species share one inferred "mechanisms" such as phyletic slide or more common limiting resources. Of course, and recurvation, and, perhaps most seriously, the inferring the ecological preferences of long-extinct misuse of the population-level concept of selection plants can be an obtuse exercise, but it is possible pressure, treating it as a creative force rather than (e.g. Scott, 1978; Bateman, 1991; Phillips and as a short-hand term describing the process of DiMichele, 1992). Certainly, such inference is sorting existing alleles by natural selection. In fact, essential if paleobotany is to develop credible the plant fossil record has rarely been used to explanations for the evolution of plant form. enlarge our understanding of evolution as a bona Ecology is even more central in attempts to use fide process. fossil plant data to test or elaborate evolutionary With the rise of cladistics and other explicit theories. To use the classic analogy of Hutchinson means of objectively assessing relationships (Stein (1965), organisms are the actors in a great evolu- et al., 1984; Stein, 1987; Crane, 1990; Bateman tionary play, and ecology is the (ever-changing) et al., 1992; Doyle and Donoghue, 1992; Gensel, stage. 1992; Nixon et al., 1994) the potential circularity In this essay we adopt an unashamedly critical between phylogeny reconstruction and evolution- and polarized position on the issue of evolutionary ary inference has been broken. In theory, modem dynamics, stressing broad macroevolutionary pat- phylogenetic methods permit a pattern to be deter- terns over examples of intra-generic speciation. mined without specific mechanistic assumptions; Our objective is not to deny gradual microevolu- explanatory hypotheses compete post hoc for tion. Rather, we wish to emphasize the role of the best phylogenetic fit. Admittedly, analysis of ecology in dictating new and sometimes altemative pattern rarely specifies a single evolutionary pro- explanations for significant events in plant evolu- cess; rather it constrains the range of possibilities tion. Sadly, paleobotany barely participated in the by falsifying some potential processes (e.g. great punctuated equilibrium debate of the 1970s FrumhoflF and Reeve, 1994; Leroi et al., 1994). At and 1980s. Now that ecology has come of age in W.A. DiMichele, R.M. Bateman/Review of Palaeobotany andPalynology 90 (1996) 223-247 225 paleontology, paleobotanists again are presented plants, arguably the most profound evolutionary with an opportunity to integrate the plant fossil diversification in land-plant history, demonstrates record with basic studies of evolutionary processes. that radiations can be self-limiting, constrained by This can be done only by escaping the constraints the interaction of ecospace and morphological of theoretical orthodoxy, notably the uncritical complexity. acceptance of insensibly gradual, competitively driven evolutionary change without serious consideration of the important ecological component. 2. Case study I: Ecological constraints on adaptive scenarios — evolution of heterospory and the seed 1.2. Scope and objectives habit

The goal of this essay is to examine the role of 2.1. Background: the nature of heterospory paleoecology in constructing evolutionary explanations for taxic-phylogenetic, morphological, and With the exception of the tree ferns, nearly all biogeographic patterns. We will advocate greater numerically abundant and taxonomically diverse awareness of the vast amount of accessible ecologi- Imeages of trees have been heterosporous. This cal data and incorporation of "ecological think- observation demonstrates irrefutably that hetero- ing" into paleobotanical scenario-building. thallic heterospory, in which male and female sex Typical use of the term "ecology" is undesirably organs are produced on separate gametophytes general; it can refer to the autecologies of mdivi- derived from small and large sized spores, respec- dual species, the central environmental tendencies tively (for detailed terminology see Bateman and of an entire clade of organisms, or the dynamic DiMichele, 1994b), confers significant ecological interactions of species at the conmiunity, land- advantages. Phylogenetic patterns suggest that het- scape, or biome levels. Excluded, however, erospory evolved independently at least ten times are speculations about environmental "selection among vascular plants (Bateman and DiMichele, pressures" as creative forces. Ecological con- 1994b; Bateman, 1995), including the zostero- siderations, when inferred independently of the phylls, selaginellalean plus rhizomorphic lycopsids, organisms in question, can constrain evolutionary equisetaleans, several filicalean ferns, and several scenarios in many ways, some obvious but others progymnosperms plus their descendants, the seed more cryptic. Our chosen examples focus on two plants (Fig. 1). Thus, there was no single case of areas. directional selection generatmg a highly adapted First, in reconstructing the controls on major heterosporous Uneage from which all subsequent morphological transformations, environmental heterosporous lineages diverged. The strongly iter- information may modify the interpretation of the ative nature of the life history lends credence to timing and causes of morphological differences the view that it is an inevitable outgrowth of between presumed ancestor and descendant (s). homosporous ancestors and that it confers a sig- The evolution of heterosporous plants from homo- nificant adaptive advantage (e.g. Chaloner and sporous ancestors and the ultimate evolution of Pettitt, 1987). seed plants serve to test the idea of a progression Inspection of the fossil record leads to three of biologically superior (or better adapted) life generally accepted conclusions: heterospory is an histories. evolutionarily successful life history, free-sporing Second, the fossil record contains important heterospory is clearly derived relative to homo- examples of major evolutionary radiations in spory (as is the seed habit relative to heterospory, which both the stem lineages and the limits of a however these terms are defined), and the homo- morphological envelope are established early, fol- spory-heterospory-seed habit transition sequence lowed by relatively routine filling of the morpho- represents a progressive increase in reproductive logical space via less profound speciation events. sophistication (Table 1). The evolution of the seed The Devonian-Mississippian radiation of vascular has been the focal point of a series of intermittently 226 W.A. DiMichele, R.M. Bateman/Review of Palaeobotany and Palynology 90 (1996) 223-247

Seed-Plants

Ma B.P. 1 5 300 0. STEP

CO WEST

320 - o NAMU LU LL GYMNOSPERMOPSIDA z o VISE 340 _ CO < o TOUR 360 STRU FAME

^ FRAS

380 - = GIVE z EIRE EMSI lU SIEG Q 400 - GbUI •jfi Questionable identity of ancestral class PRID COOKSONIOPSIDA ^ Questionable monophyiy LUDL of descendant class 420 TRACHEOPHYTA s.l. WENL CO

Fig. 1. Tentative non-numerical phylogeny of all tracheophyte classes, showing putative ancestor-descendant relationships plus divergence dates, and occurrence of heterospory. Note that (1) the entire post-cooksonioid radiation occurred within the Devonian, and (2) a minimum of ten independent origins of heterospory is indicated by the stippling, taking into accoimt recent assertions of monophyiy for the Salviniales plus Marsileales based on morphological (RothweU and Stockey, 1994) and molecular (e.g. Hasebe et al., 1994) data. (/) Some Barinophytales; (2) all Sellaginellales plus all rhizomorph-bearing lycopsids (Isoetales s.l.); (5) some Equisetales; (4) some Spbenophyllales (doubtful); (J) some Stauropteridales; (6) all Hydropteridales (Salviniales plus Marsileales); (7) some Filicales (e.g. Platyzoma); (5) some Aneuophytales; (P) some Archaeopteridales, ?all Protopityales, all Cecropsidales; (70) some Neoggerathiales. (Modified after Bateman and DiMichele, 1994b, fig. 11.) contentious debates (Thomson, 1934; Andrews, and Serbet, 1994). Heterospory has received less 1963; Pettitt and Beck, 1968; Pettitt, 1970; Steeves, conceptual attention (Willson, 1981; Haig and 1983; Chaloner and Pettitt, 1987; DiMichele et al., Westoby, 1988b; DiMichele et al., 1989; Bateman 1989; Chaloner and Hemsley, 1991). Recently, the and DiMichele, 1994b), and most paleobotanical increasing rigor of phylogenetic reconstructions scenarios have treated it merely as an intermediate has sharpened the debate on ancestry (Meyen, stage in the evolution of the seed. 1984; Beck, 1985; Stein and Beck, 1987; Donoghue, Nearly all studies of the evolution of heterospory 1989; Donoghue and Doyle, 1989; Galtier and have focused on structure alone. Little attention Rowe, 1989; Crane, 1990; Doyle and Donoghue, has been paid to the ecological preferences of the 1992; Bateman and DiMichele, 1994b; RothweU taxa or life histories in question, or even to the JV.A. DiMichele, R.M. Bateman/Review of Palaeobotony andPalynology 90 (]996) 223-247 227 breadth of variation in the ancestral, supposedly 1988a; Shefiield, 1994; Bateman and DiMichele, primitive homosporous condition. This problem 1994b) indicates a wide range of variation within has been compounded by an insistent desire to the basic homosporous pattern of alternation of place all known morphological fonns (or classes free-living generations. For example, in many fern of forms) into continuous progressions, despite the species the gametophytes rely on chemical signals lack of formal phylogenetic support for such (antheridiogens) to mediate population-level sex schemes (Andrews, 1963; Tiffney, 1981; Chaloner ratios and control the timing of gametogenesis and and Pettitt, 1987; Chaloner and Hemsley, 1991). syngamy, and in most species at least some gameto- These scenarios are rooted in an acceptance of phytes retain their potential for self-fertilization. gradual transformation of form, driven by "selec- Thus, the gametophyte generation is closely tive pressures" for functionally superior morpholo- attuned to local environmental conditions and can gies. The foremost assiunption of this form of effectively regulate its reproductive functions. The gradualism is competition. Successive, increasingly main disadvantage of homospory seems to be complex morphologies must be competitively supe- the need for ecological coordination between the rior to the ancestral forms, and increase in com- gametophyte and sporophyte generations. In par- plexity must be associated with increase in fitness. ticular, the sporophyte must grow at or near the However, for competition to favor the rise of point of syngamy, a location dictated by the the advanced architectures at the expense of the gametophyte. Thus, evolution away from the norm primitive ancestral forms, there must be Httle or of mesic, moist environments is unusual. The evo- no ecological differentiation between ancestor and lution of aquatic-amphibious habit on the part of descendant. Unfortunately, the details needed to both sporophyte and gametophyte seems to have fit this view to even the most rudimentary evolu- been particularly demanding once a fully terrestria- tionary models are rarely given. Are such trans- lized, homosporous life history was estabUshed. formations allopatric, or is mass selection across "Return" to the water requires niunerous changes entire species involved? What are the environmen- in morphology and physiology of both sporophyte tal conditions imder which the transformation and gametophyte. However, as free-Uving, inde- occurred, and what kinds of advantages are con- pendent Ufe history phases, regulation of develop- ferred by the derived morphologies under those ment and phenotype, and the selective factors circumstances? acting on that phenotype are partially (largely?) independent, even though the two phases share a 2.2. Ecological constraints and the homospory- common genome. Increased terrestrialization, in heterospory transition contrast, is limited mainly by syngamy, which can be accommodated in many ways, including Heterosporous plants evolved from ancestors through apomixis. Overall, therefore, homospory that possessed a remarkably flexible and ad- is an effective life history in terra firma habitats. vanced reproductive strategy, namely homospory Limits on homosporous ferns, lycopsids, and (Table 1). A survey of recent literature on extant sphenopsids in modem habitats may reflect the pteridophytes (Willson, 1981; Haig and Westoby, limitations of vegetative architecture and "house-

Table 1 Characteristics of four categories of vascular plant life histories

Gametophyte Dominant phase Sex ratio (?/? control: timing of Functional dependence gametogenesis of tJ/$ on ®;

Homospory Free living Codominance Labile Labile, (J/$ controlled Independent Anisospory Free living Codominance Fixed Labile, (J/? controlled Independent Heterospory Endosporic Sporophyte Fixed Mainly ® controlled Independent Seed habit Endosporic Sporophyte Fixed AVholly ® controlled Dependent 228 W.A. DiMichele, R.M. BatenumIReview of Palaeobotmy and Palynology 90 (1996) 223-247 keeping" physiology more than reproductive biol- respond to environmental variabiUty, including ogy. The common view of homospory as an conditions unfavorable for gametogenesis, is to inferior life history waiting to be displaced is enter diapause (suspended development) inunedi- difficult to justify, particularly in mesic habitats. ately after release and before "germination" (note In contrast with homospory, the gametophytes that this ability was probably available in their of heterosporous plants are strictly unisexual homosporous ancestors - spores of most extant (Fig. 2). Sex ratios are determined by the sporo- ferns accumulate in the soil as spore banks; Dyer phyte epigenetically (developmentally rather than and Lindsay, 1992). This is a remarkably inflexible through sex chromosomes) during sporangial mat- life-history strategy, given that spores are released uration. In effect, microspores and megaspores directly into the environment without the potential function as gametes. The way gametophytes to form a photosynthetic, free-living, indepen-

TERRA FIRMA HABITATS AQUATIC —AMPHIBIOUS HABITATS

HOMOSPORY •• -^and^ must independently acquire "^and^ haveI traits that confer similar environmenta aquatic function requirements but HETEROSPORY independent development •^ must acquire traits that confer aquatic function limited ^ flexibility requires apomictic reproduction pollination

-^functions as unitary SEED HABIT organism that adapts to environment delivery of O directly toy circumvents environmental limitations to syngamy

Fig. 2. Constraints on life history evolution in terra firma and aquatic-amphibious habitats, as the sporophyte gradually co-opts the gender control previously exercised by the gametophyte. Note especially the ineffectiveness of (1) homospory in aquatic- amphibious environments and (2) heterospory in terra firma habitats without apomixis or reliable pollination. Dotted lines indicate transitions that have been rare in plant history due to ecological constraints. Solid lines suggest the morphological-ecological history leading from homosporous plants to seed plants. W.A. DiMichele, RM. Bateman/Review of Palaeobotany andPalynology 90 (1996) 223-247 229 dently self-supporting individual. How then did anything more than an evolutionary curiosity, it free-sporing heterosporous plants become success- nonetheless has risen to cult status. However, ful ecologically? Current evidence suggests that survey of the modem flora reveals no other exam- heterosporous plants have been ecologically domi- ples of this life history. Examination of the ecologi- nant only in environments with ample free mois- cal implications of the platyzomoid life history ture, notably aquatic and amphibious habitats. In indicates that heterospory with free-Uving gameto- such environments spores-as-gametes are most phytes bears all the disadvantages of both homo- likely to encounter conditions favorable for fulfill- spory and heterospory with the advantages ing their function, though even here the extant of neither: the ecological-evolutionary tension Salviniaceae and Marsileaceae possess sophisti- between the sporophyte and gametophyte remains, cated sporocarps that allow a resting phase and the gametophytes are xmable to adjust the sex following sporogenesis. Admittedly, some species ratio and timing of reproduction in response to of extant heterosporous plants grow in mesic to environmental cues. If other such "intermediates" xeric habitats, but in these environments apogamy existed they are Ukely to have occurred as small, predominates (DiMichele et al., 1989; Bateman ephemeral populations and, therefore, on statisti- and DiMichele, 1994b). cal principles alone were unlikely to survive for What advantage is conferred by a free-sporing long periods. Allopatric isolates may be common heterosporous mode of reproduction? The most products of the dynamics of the evolutionary pro- obvious characteristic is unity of form. The sporo- cess, but few appear to survive to establish long- phyte is the dominant phase of the life cycle and lived clades; the ecological handicaps of the becomes the focus of selection on vegetative func- platyzomoid life history thus combine with the tion and environmental tolerance (Table 1, Fig. 2). chance elements of evolution to make it doubly However, because the gametophytes and gametes unlikely that such derived lineages would foimd must be released into the environment, the gameto- new clades. phyte generation continues to constrain the condi- Homospory in modem lower vascular plants tions under which the system can function encompasses a complex array of functional mor- effectively. In gaining the advantages of a com- phologies, some quite sophisticated in their control pressed life cycle, the potential to colonize terra of sexual reproduction. Most of the biochemical firma habitats is severely curtailed by the sporo- adaptations found in extant fems could not be phytically fixed sex ratio, the inability of gameto- recognized in the fossil record. However, there is phytes to adjust to most environmental vagaries, no reason to caricature Devonian homosporous and the strict requirement for moisture during plants. By today's fiUcalean standards, tie life spore germination and syngamy. history represented by Platyzoma is functionally Although many reviewers have appealed to an inferior to the complex life histories typical of "intermediate" evolutionary stage between homo- many homosporous species. If complex homospo- spory and heterospory (of the heterothallic, endo- rous Ufe cycles evolved during the Devonian, free- sporic variety), we regard heterospory with free- living heterospory is an unlikely intermediate form living gametophytes as one of the great paleobo- in the evolution of heterospory, simply on ecologi- tanical fantasies. These are imagined intermediate cal grounds. forms between homosporous ancestors and each of the independent origins of heterospory. In most 2.3. An ecological perspective interpretations of neo-Darwinism, first principles dictate gradual transformation of form and hence Heterospory is ecologically successful in a an insensible series of intermediates. A supposed different set of environments than homospory. The vindication of that expectation was the discovery heterosporous life history is advantageous in of a rare filicalean fern Platyzoma (Tryon, 1964) aquatic and amphibious habitats where gameto- that possesses such a life history. Although Sussex phytes are assured of favorable conditions; hetero- (1966) soon warned against treating Platyzoma as sporous plants in drier habitats generally are 230 W.A. DiMichele, R.M. BatemanIReview of Palaeobotany andPalynology 90 (1996) 223-247 apomictic (Fig. 2). In contrast, homospory is permitted escape from competition (or, in other rare in aquatic habitats (the semi-aquatic fern terms, exploitation of a new resource). Ceratopteris is an interesting exception that can complete its life cycle rapidly under aquatic condi- 2.4. Evolution of the seed tions; Tryon and Tryon, 1982; Eberle et al, 1994). The extended gametophytic life-span of almost all The earliest known seeds occur in Late Devonian homosporous plants permits a wider range of swamp habitats (Gillespie et al., 1981), providing response in terra firma habitats. Nevertheless, the evidence that early seed plants preferentially occu- great differences in sporophytic and gametophytic pied the same kinds of environments that were form, and the continued requirement for surface exploited by their heterosporous ancestors. moisture to effect fertilization, restrict the abiUty However, the great diversity of early seed plants of homosporous species to radiate into aquatic and seed morphologies occurs in terra firma habitats. As with heterosporous lineages, homo- habitats (Andrews, 1963; Long, 1975; Scott, 1980; sporous plants have been able to expand to the Retallack and Dilcher, 1988; Rothwell and drier end of the environmental spectrum. Scheckler, 1988), suggesting that seed plants radi- The transition to the aquatic-amphibious habi- ated primarily in drier habitats. As with the tat is especially demanding. The need to modify homospory-heterospory transition, competitive evolutionarily both the sporophyte and gameto- superiority has often been invoked in the hetero- phyte appears to have been a major factor that spory-seed habit transition. In both cases, rudi- prevented homosporous plants from exploiting mentary ecological analysis offers little support to such environments. Thus, endospory is the single the a priori hypothesis of competition. most important breakthrough that permits the Perhaps the most serious issue in considering the evolution of seed habit is its definition. Almost invasion of aquatic habitats (Bateman and universally, seed habit is defined as a heterosporous DiMichele, 1994b). Endospory leaves the sporo- condition in which the number of functional mega- phyte to face the vagaries of the environment. spores per megasporangium has been reduced to Only during reproduction must the gametophytes one. The one viable spore develops completely be released, and then only for a brief period. But within the megasporangium, which is surrounded it is this reproductive phase, despite the compres- by additional tissue that is generally considered to sion of the developmental stages between meiosis be of sporophytic origin. As a consequence of this and syngamy, that restricts the choice of habitats, morphology, the male gametophyte, also endo- just as it opens the aquatic habitat to invasion. sporic in development, must be deUvered to the We see no need to advance intermediate forms seed, a process termed pollination. Most studies between homospory and endosporic heterospory, of seed evolution have focused on the elaboration and have argued elsewhere (DiMichele et al., 1989; of the integimients (Andrews, 1963), on the rela- Bateman and DiMichele, 1994a,b) that the mor- tive efiiciency with which various early forms cap- phological transformation is developmentally con- ture pollen (Niklas, 1981), or on likely ancestry trolled and thus can yield a "hopeful monster" (Beck, 1985; Crane, 1990; Rothwell and Serbet, in a single generation (see also Van Steenis, 1969; 1994). The evolution of the seed habit itself has Arthur, 1984; Levin, 1993). Ecologically, early been addressed only tangentially, via conceptual heterosporous forms probably entered and gradualist arguments in which the seed is assem- exploited an environment virtually unoccupied by bled step-wise through a now familiar series of other vascular plants. They were capable of passing morphological intermediates. Such scenarios con- through a selective filter almost impenetrable to stitute an evolutionary argument only if gradual- homosporous plants. Consequently, there is no ism is again considered axiomatic, and if the final reason to invoke competitive superiority to explain configuration of the seed is regarded as an optimal, the evolution of heterospory from homospory. stable morphology that is more likely to resist Rather, it can be viewed as a happenstance that further evolutionary modifications than any of the fV.A. DiMichele, KM. BatemanjReview of Palaeobotany andPalynohgy 90 (19%) 223-247 231 so-called "intermediate" forms. Once more, how- 1994b). It was their ability to reproduce under a ever, most of the critical intermediates are missing wide range of conditions that enabled them to from the fossil record; either they have not yet exploit parts of terra firma enviroimients exploited been detected or they never existed. by few homosporous plants. In addition, the bifa- From an ecological perspective only one "step" cial cambiimi of seed plants, permitting massive in this transformation is critical to the life history wood production while retaining effective photo- we view as the seed habit, namely delivery of the synthate transport, may have allowed them to male gametophyte directly to the female. Thus, partition terra firma habitats in ways not pre- pollination is the key innovation, less from a viously possible. Their reproductive methods morphological perspective than an ecological one. allowed them to pass the filter between aquatic- Plants with routine pollination have come as close amphibious and terra firma settings, but it was to unifying the sporophyte and gametophyte into primarily vegetative specialization ("economic a single individual as can be achieved by sessile factors" sensu Eldredge, 1989) that facilitated their organisms (Bateman and DiMichele, 1994a,b). exploitation of drier habitats. The gametophytes no longer place environmental When ecological factors are considered it restrictions on the sporophyte, which becomes appears that seed plants may have come into limited largely by vegetative environmental toler- competition with heterosporous plants-and lost! ances rather than constraints on reproduction. It The first seed plants grew in enviroimients aheady would be impossible to distinguish this break- heavily saturated with heterosporous species (par- through in the fossil record, due to the diflBculty ticularly lycopsids and progymnosperms) as place of distinguishing free-sporing "heterosporous" holders. Although some species may have become plants from structurally similar plants experiencing estabUshed, the fossil record demonstrates that routine pollination. seed plant species failed to dominate aquatic- It is Hkely that the first plants with pollination amphibious environments until the latest evolved within the aquatic-amphibious habitats Paleozoic. In contrast to their origin, the early occupied by their heterosporous predecessors radiation of seed plants may have occurred under (Fig. 2). The fossil record documents that seed conditions of relatively Uttle competitively medi- plants did not achieve dominance in these environ- ated selection (note that this also apphes to ments until late in the Paleozoic. Rather, the most several earlier radiations of heterosporous species). rapid increase in seed-plant diversity in terra firma Pollination was a "pre-adaptation" that permitted habitats occurred through the Late Devonian and a major switch in the ecological amphtude of an Early Carboniferous, where it rapidly became the entire clade, a bona fide key innovation (a morpho- dominant life history. Heterosporous plants con- logical or physiological innovation that permits a tinued to dominate wetland habitats until removed clade to switch resources and escape competitive by extrinsically induced extinction (Phillips and constraints). It was not until abiotically driven Peppers, 1984; DiMichele and Aronson, 1992). extinctions eliminated heterosporous tree forms Enviroimiental place holding on ecological time- that seed plants were able to colonize aquatic- scales was termed "home-field advantage" by amphibious habitats. Pimm (1991). It seems that the pattern can be It could be argued that the radiation of several extrapolated to geological time intervals, especially distinct heterosporous clades in wetlands during at the level of higher taxa. As we will discuss in the Paleozoic (Fig. 1) contradicts the argument our second case study, the seed plant radiation that home-field advantage should dissuade may have been suppressed in aquatic-amphibious multiple radiations of similar life history stategies habitats by the already well established occupancy in similar habitats (B.H. Tiffney, pers. commun., of earlier heterosporous plants (Knoll and Niklas, 1994). However, the radiations in aquatic-amphib- 1987). Certainly, the earliest seed plants probably ious environments are an edaphic complex of had similar vegetative tolerances to their hetero- habitats, and thus offer a number of niches for sporous precursors (Bateman and DiMichele, exploitation; they effectively constitute a biome. 232 W.A. DiMichele, R.M. Bateman/Review of Palaeobotany and Palynology 90 (1996) 223-247

Freshwater aquatic-amphibious habitats also are the "zygopterid" and filicalean lineages (Chaloner isolated relative to most drier terrestrial habitats, and Sheerin, 1979; Scott, 1980; Stein et al., 1984; offering more opportunity for local estabUshment Galtier and Scott, 1985; Meyen, 1987; Crane, of derived clades. Although several, mainly lower- 1990). Within-clade radiations lagged behind by vascular plant groups radiated within wetlands about one geological stage but conformed to the during the Paleozoic, most of these radiations basic architectural themes established in the earlier produced limited numbers of taxa. The seed plants major diversification (but note that this lag may were no exception to this rule; the radiation of be explained partly by sampling of species in the this group in aquatic-amphibious settings pro- fossil record: on average, a class will be more duced few taxa. It was not until they entered drier readily detected than an order; D.H. Erwin, pers. habitats that a major radiation took place. The commun., 1984). The radiation of the angiosperms aquatic-amphibious environment of the Paleozoic is the final (and ongoing) diversification of vascular offered limited opportunity for radiation due both plants; it has resulted in several architectural forms to physical restriction and the presence of numer- not represented in the earlier radiations, such as ous occupants. monocotyledonous vegetative organization and the Unlike the heterospory-homospory transition, herbaceous habit, though we regard these as rela- no catastrophic structural changes are required in tively minor modifications of the earlier seed-plant the heterospory-seed habit transition. Rather, the bauplan. structural modifications that are so well docu- Figs. 1 and 3 show that the Devono-Carboni- mented in the fossil record are mere postscripts to ferous radiation established what traditional seed plant origins. Certainly, integumentation Linnean taxonomy has regarded as classes of affects pollination efficiency and enhances gameto- vascular plants: Lycopsida, Sphenopsida, phyte protection, and various micropylar and Pteropsida, Progymnospermopsida, Spermato- cupule modifications were instrumental in the radi- psida (we here follow the taxonomic system of ation of seed plants. But an understanding of the ICnoU and Rothwell, 1981). The phylogenetic patterns of change through time in these accessory studies of Crane and colleagues (Crane, 1990; structures does not lead to a greater understanding Kenrick and Crane, 1991) have provided informal of the origin of this subsequently dominant life names that capture more accurately the phyloge- history. netic structure of the relationships, and conform broadly to the traditional Linnean taxa. In effect, Linnean higher taxa are short-hand for the distinc- 3. Case study 11: The radiation of vascular land tive vegetative and reproductive architectural char- plants and the emergence of the ecological hierarchy acteristics that separate the major clades. The degree of phylogenetic resolution is highly 3.1. Major land-plant radiations variable both within and between major clades. The pattern attending the origin of the sphenopsids By the end of the Early Carboniferous, ter- is the best studied. Stein et al. (1984) showed that restrial vascular plants had undergone two of the the sphenopsids originated from an as yet incom- three major radiations evident in the fossil record pletely resolved pool of potentially ancestral forms. (Fig. 1). The first occurred during the Siluro- Although the broad patterns of descent are clear Devonian and gave rise to the cooksonioids, zost- for groups other than the sphenopsids, transitional erophylls, lycopsids, rhyniophytes, and trimero- morphologies have not been found that clearly phytes (Banks, 1975; Grensel and Andrews, 1984; link specific sublineages. In particular, ancestral Knoll et al., 1984; Niklas et al., 1985). The second homosporous lycopsids or trimerophytes are not spanned the Late Devonian-Early Carboniferous well connected to the derived clades, such as the and generated the selaginellalean and rhizomor- rhizomorphic lycopsids, the various fern lineages, phic lycopsids, sphenopsids, progymnosperms, or the progymnosperms. Relationships between seed plants, and several "fern" groups, including the wholly extinct progymnosperms and the puta- W.A. DiMichele, KM. Bateman/ReviewofPalaeobotanyandPalynology90 (1996) 223-247 233 tively descendant seed plants remain contentious. randomly across physical habitats; rather, the radi- The many morphological and phylogenetic studies ation was characterized by strong clade-environ- have all been handicapped by the paucity of fully ment interactions. Chaloner and Sheerin (1979) reconstructed progymnosperms. As indicated by documented the preceding accumulation of mor- the sphenopsids, the Late Devonian was a time phological innovations diuing the Devonian, and of wide-ranging morphological innovation. The Banks (1980) provided a biostratigraphic context "morphological envelope" was largely circum- for the major taxa. Knoll et al. (1984) described scribed during this time; it was filled during subse- patterns of diversification during the Devonian quent lower level radiations, which played on the and, most significantly, quantified the degree of major structural themes that had already evolved morphological differentiation among the major (Bateman, 1991). This potentially fractal taxo- groups. Knoll and Niklas (1987) argued for a nomic pattern is evident in the early class level quantitative adaptationist approach to evaluating radiation and subsequent order level radiations evolutionary scenarios that encompassed biomech- summarized in Fig. 3, though a more rigorous anical attributes of organisms but lacked a detailed analysis extended to lower taxonomic levels is paleoecological component. More explicitly eco- desirable (cf. Erwin et al., 1987). logical studies, focusing mainly on floristics, Surprisingly little ecological attention has been include those of Scheckler (1986a,b), Bateman devoted to this fundamental class-level radiation. (1991), and Scott and coworkers (for summary Most discussion has centered on the evolution of see Scott, 1990). Retallack and Dilcher (1988) particular morphological features, such as the tree examined the ecological implications of inferred habit, vascular morphology, or seeds. This focus Early Carboniferous seed-plant biologies, and overlooks their more profound context as part of Raymond (1987) evaluated the paleobiogeo- the evolution of nearly all major architectural graphic distribution of major morphological traits. plans in vascular plants, an event that occurred Several studies used a range of approaches to during a remarkably short period relative to the evaluate phylogenetic relationships (e.g. Chaloner total history of the tracheophytes. The literature and Sheerin, 1979; Knoll and Rothwell, 1981; on this interval and its evolutionary history is Meyen, 1984; Stein et al., 1984; Crane, 1988). It broad; key papers are summarized below. Many is from the totality of approaches that a picture taxonomically restricted features did not occur of the radiation emerges.

3.2. Questions of scale

We will briefly review the literature relevant to the ecological implications of the Devono- Carboniferous radiation. Invertebrate and vertebrate paleontology have developed many concepts that are broadly appUcable to interpretation of patterns in the plant fossil record. Suggestions that plant and animal evolution were guided by different suites of mechanisms should be scruti- S/DDLCUCP'R JKTB nized in light of existing theory. The basic shapes Fig. 3. Timing of origination of class and order level taxa of basal radiations, the nature of morphological indicated by the fossil record. Ordinal level originations peak discontinuity among lineages, and the basic tenets later and are far more extended. Classes are Cooksoniopsida, of speciation are the same for plants and animals. Rhyniopsida, Trimerophytopsida, Zosterophyllopsida, Lycops- The literature review that follows is intended to ida, Progymnospermopsida, Cladoxylopsida, Sperma- topsida, Sphenopsida, Pteropsida (see Fig. 1). Orders from emphasize existing explanatory models that apply Knoll and Rothwell (1981); angiosperms are treated as as well to plants as to the animals on which they an order. were formulated. Crucial questions about the class- 234 IV.A. DiMichele, KM. BatemanIReview of Palaeobotany andPalynology 90 (1996) 223-247 level vascular plant radiation are, what caused it space because they were likely to have very low to begin and what caused it to end? We will argue fitness and little competitive ability. Valentine's that upward causation is the key, especially the model predicted that ecospace existed indepen- degree to which processes operating at the scale of dently of the occupying organisms. It was most local populations within communities can account widely available at the onset of a radiation and for the phylogenetic shape and ecological rapidly filled as it became colonized via major consequences of a major phenotypic radiation. phenotypic jumps (Fig. 4). Subsequent speciation It appears likely that the ecological spatio- tended to deviate progressively less from the ini- temporal hierarchy with which we are famiUar tially estabUshed architectural themes because (community > landscape >biome) did not exist in there were no low-competition ecological voids the Late Devonian, but evolved in concert with that could accommodate major phenotypic the morphological radiation. As it developed, the change. hierarchy began to constrain (or perhaps contain) This type of radiation was classified by Erwin the spatial and temporal ranges over which popula- (1992) as a "novelty" event: one that takes place tion-level processes could act, and thus increasingly under low selection and involves organisms with channelled the vascular plant radiation. weak genetic and architectural constraints. The Valentine (1980) suggested that during the early novelty radiation is followed by more typically Paleozoic radiation in marine ecosystems specia- "adaptive" radiations within the limits of the tion was limited by the availabiUty and size of ecological space occupied by the founding lin- "empty" niche space. Organisms exhibiting minor eage(s). Erwin (1992) noted that in the fossil functional modifications needed only small low- record of marine invertebrates events of this type competition ecospaces in which to estabhsh tended to occur in the Paleozoic, presumably themselves, whereas carriers of major structural because empty ecological space was more common or functional deviations needed larger voliunes of then, and because genomic and developmental

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Fig. 4. Hypothetical pattern of rapid occupation of the available ecospace following class-level originations in the Siluro-Devonian. Squares represent "adaptive" space (tesserae in the model of Valentine, 1980). Founders of a major clade require more adaptive space than subsequent speciation events that are smaller scale modifications of that same basic theme. Space filling combines with progressive canalization of development and architectural constraint to limit both the opportunity for survival of highly divergent forms and the likelihood of their occurrence. W.A. DiMichele, R.M. Bateman/Review of Palaeobotany andPalynology 90 (1996) 223-247 235 constraints were less entrenched, permitting more explicit with regard to the all-important level in phenotypic variation. In Valentine's scenario there the organismal hierarchy at which constraints is a progressive interaction between morphological operate. change (the engine of which is not of immediate The interaction of ecological and evolutionary concern; it is assimied that a spectrum of variation, dynamics on long time scales also has been from tiny differences to large discontinuities, is addressed by other workers. As detailed by Vermeij present at all times) and ecological space, even (1987), the concept of escalation explicitly requires though the ecological space is regarded as largely environmentally forced ecological disruption to predefined. Fundamentally, the ecological factors break up co-evolved species complexes. Such of standard neo-Darwinian evolution (principally, complexes effectively exert home-field advantage the chance location of a suitably low competition and exclude "invaders" from access to resources. site by a population bearing a derived phenotype, Extinctions open up resources and permit compar- generally via an allopatric event) are those con- atively brief bursts of competitively driven evolu- trolling speciation, irrespective of the degree of tion. Brett and Baird (1995) provided perhaps the phenotypic deviation from the ancestor. most explicit link between landscape- and biome- Significant parts of Stanley's (1975, 1979, 1990) level changes in marine faunas and synchronous, "species selection" paradigm also focus on the macroevolutionary changes in many of the compo- interaction of extinction and origination rates in nent lineages. They argued that early Paleozoic evolving lineages and thus treat ecological factors faunas persisted taxonomically and structurally for as at least partially dependent on biotic factors. several million years. Periods of persistence were Stanley demonstrated that high rates of speciation terminated by brief intervals of rapid turnover, (as opposed to origination, which was assimied to accompanied by the emergence of new ecological be stochastically constant) within clades must be structures. Major evolutionary divergences were accompanied by high rates of extinction, and that concentrated in several Uneages during these large population sizes tend to reduce the likelihood intervals of ecological disequilibriiun; these were of speciation. Both factors reflect the inter- "ecologically induced" radiations sensu Erwin actions of speciation and adaptive (niche) space. (1992). Simpson (1944) viewed major phenotypic Origination may provide a wide range of variation changes as rapid shifts from one adaptive peak to for selection but there also must be sufficient another (this is consistent with the pattern outlined adaptive space to allow the establishment of small in Fig. 4). Calling such changes "quantum evolu- derived populations. Without extinction, pheno- tion", Simpson visualized a causal combination of typically derived forms tend to encounter ecologi- happenstance attainment of a threshold level of cally similar ancestors; generaUsts with large "pre-adaptation" coinciding with unusually great population sizes are on average more resistant to ecological opportunity. Simpson (1953) later extinction, so these groups tend to occupy extens- brought these concepts more in line with standard ive ecospace for relatively long periods and have neo-Darwinian models of allopatric speciation, relatively low speciation rates. which implicitly require an ecologically uniformi- Damuth (1985) argued for a more clearly pop- tarian viewpoint. ulation-centered, and hence more ecologically cen- In contrast to models in which ecology is implic- tered, formulation of species selection; selection itly or explicitly central, most macroevolutionary among species takes place through the mteractions models have focused on the origin of variation, or of "avatars": local community-specific populations on the "internal" morphological constraints to of larger species ("ecotopodemes" sensu Gilmour phenotypic change, in which ecology plays a role and Heslop-Harrison, 1954). In Damuth's formu- only as a final, passive selective filter (sensu lation avatars are to species as individuals are to Rothwell, 1987). Several authors (e.g. Bateson, populations. They provide the basis for an ecologi- 1894; Goldschmidt, 1940; Schindewolf, 1950; and cal analysis of selection among species, a model later Eldredge and Gould, 1972; Gould and broadly consistent with that of Stanley but more Eldredge, 1977; Gould and Lewontin, 1979; Stidd, 236 W.A. DiMichek, R.M. Bateman/Review of Palaeobotany and Palynology 90 (1996) 223-247

1980; Arthur, 1984, 1987; Levinton, 1988; Gould, are always appearing, but their probability of long- 1991; Stebbins, 1992) looked for developmental term survival decreases rapidly as ecospace occupa- factors to explain the alternation of short-term tion increases; consideration of constraints phenotypic change and long-term phenotypic enforced by increasing developmental complexity stasis. Such models view evolution within lineages alters this expectation, reducing the expected as constrained principally by "historical" events, breadth of divergences. A consequence of this i.e. architectures created in the past that persist model, which we discuss below, is that the ecologi- into the present (Gould and Lewontin, 1979; cal hierarchy evolves in complexity and connectiv- Gould and Vrba, 1982). Early, morphologically ity as a major radiation proceeds. In doing so, it wide-ranging radiations are argued to be a con- begins progressively to constrain that radiation in sequence of poorly canalized developmental path- a negative feedback loop. ways and limited interactions among the architec- All of these macroevolutionary scenarios, tural components of organisms. The fixation of whether or not they include an ecological compo- Uneages and architectures early in a radiation is nent, contrast with the gradualism taken as the thus strictly a consequence of ever-mounting default in most paleobotanical forays into evolu- constructional "burden" (sensu Riedl, 1979) and tionary biology, the most obvious example being ever more complex developmental interactions Zimmermann's (1959) unduly influential Telome (Gould, 1977). Theory. Gradualist models are perhaps more Erwin and coworkers (Erwin and Valentine, "Darwinian" than "neo-Darwinian". They rely on 1984; Erwin et al, 1987; Erwin, 1993) argued that the assumption that the environment provides a Valentine's model needed to be modified by includ- uniform landscape across which blow prevailing ing such morphological and genetic constraints as winds, the "selective pressures" for whatever mor- those considered in more traditional formulations phological feature is under study. Guided by com- of macroevolution. Such constraints would reduce petition, organisms are assiuned to create an the likelihood of major phenotypic changes invariable backgroimd of minor phenotypic varia- through time as developmental and genomic con- tion that is subject to constant gentle selection tingencies evolved ("canalization" sensu Wadding- pressures. The result is a stately, continuous ton, 1942; see also Arthur, 1984). unfolding, not the discontinuous, fractally pat- The Devono-Carboniferous origin of major vas- terned process envisioned by most macroevolution- cular-plant architectures appears to be an Erwin- ary models (Fig. 4). The "ecological" component style "novelty" radiation. Early in such a radiation, in these graduaUst models is often in practice highly derived forms may be able to survive even merely the "selective pressures" themselves. if they have ecological tolerances vastly different from their ancestors (equivalent to biome-scale 3.3. Major plant groups: initiation of the class-level differences). High extinction rates (Stanley, 1990) radiation are not required at this stage because of low utilization of the full spectrum of resources. As "Why at that particular time?" is a question resources become increasingly saturated, derived that can be asked about any phenotypic radiation phenotypes begin to encounter "occupied" adap- at any taxonomic scale. Although the paleobota- tive space more frequently, thus selecting against nical record clearly documents an architectural the more divergent forms. Smaller-scale evolution- radiation of major proportions during the Late ary events, which were happening all along, begin Devonian and Early Carboniferous (Fig. 1), the to fill in the broad types of ecological space (e.g. vascular plant radiation has been viewed either "tropical wetlands", "regularly disturbed stream- from the perspective of phylogenetic pattern or sides"). At this point, landscapes with multiple almost completely in terms of individual attributes, communities may emerge. Again, Valentine often considered pivotal in the evolution of plants assumed that a full spectrum of phenotypic varia- (for example, the evolution of tree habit, seeds, tions are always Ukely to occur; hopeful monsters and laminar megaphyllous leaves). Competitive W.A. DiMichele, KM. Bateman/ReviewofPalaeobotanyandPalynology90 (1996) 223-247 Til interaction among plants is taken to be the driving and Sheerin, 1979). Although simple early plants force (Chaloner and Sheerin, 1979; Tiffney, 1981; possessed most of the cell types found in modem Knoll, 1984, 1986; Knoll et al., 1984; Knoll and angiosperms, diversity within particular categories Niklas, 1987; Traverse, 1988; Selden and Edwards, of cell type (e.g. meristems, vascular tissues) was 1989), and this unique Late Devonian origin of much lower. More unportantly, early land plants widely divergent, complex architectures becomes possessed few organ systems. Together, these obscured by an undesirably narrow focus on indivi- factors limited their ability to produce highly diver- dual structural components of the major plant gent derivative forms (and, by implication, offered groups. an increasing probability of producing convergent We suggest that phenotypic complexity played derivative forms). However, once a critical mass the most important role in the onset of the radia- of heritable phenotypic variability and complex tion, though detailed documentation of the asser- developmental regulation were attained, large steps tion is outside the scope of this paper. Knoll et al. could be made in the degree of divergence between (1984) made the most credible attempt to date to ancestor and descendant. In other words, the possi- document the increase in complexity that occurred bility for generating "hopeful monsters" was lim- during the Devonian (Fig. 5). For both the zoster- ited in the earliest phases of land plant evolution, ophyll and trimerophyte lineages, they detected a but became increasingly likely as phenotypes and rapid increase in morphological complexity during their regulation became more complex. This rela- the Middle Devonian, reaching a plateau in the tionship between elaboration of complex morphol- Late Devonian (and increasing again for lycopsids ogy and its developmental control underpinned in the Early Carboniferous). This implies the exis- Zimmermann's (1959) Telome Theory, which tence of a phenotypic (and hence developmental) unfortunately has yet to be satisfactorily integrated threshold of complexity that, once crossed, per- with plant developmental mechanisms as they are mitted rapid diversification-essentially complexity understood today (e.g. Stidd, 1987). begetting complexity. This threshold was reached This explanation does not rule out competition by the gradual accumulation of potentiaUy adap- as an important selective filter, though competition tive morphological structures during the early among vascular plants is indirect and is not neces- phases of vascular land plant evolution (Chaloner sarily involved in the establishment of a novel lineage (Bateman and DiMichele, 1994a) (Fig. 6). 20 Diffuse competition, perhaps landscape-scale esca- LU IX lation as envisioned to occur periodicaUy by o o ai Vermeij (1987), could have driven the entire system 1- 1 5 once complex morphologies began to appeiir. z lU z However, competition and specific selective pres- Ui o • sures alone are unlikely to account for the rela- > tively short-term structural diversification of D< vascular plants belonging to widely divergent clades, unless the organisms were ecologically s = threshold of imdiiferentiated. o complexity In this context, early land plants (Late Siltirian o I and Early Devonian) appear to have undergone a. Pr Loe 1 SI 1 Em El 1 Ql Frl Fal a. o Late*^,. Early Middle Late 1 minimal ecological differentiation. "Commimities" z SILURIANI DE VONIAN 1 commonly consisted of patchworks of monotypic stands (e.g. Andrews et al., 1977), with many of Fig. 5. Rapid increase in "morphological" advancement the species using common resources and competing following attainment of a "threshold of complexity" in the Siegenian. [Modified from Knoll et al. (1984) who listed the for the same space within streamside and wet criteria for calculation of the morphological advancement floodplain habitats (Knoll et al., 1979; Tiffney, score.] 1981; Tiffney and Niklas, 1985; Bateman, 1991; 238 W.A. DiMichele, KM. Bateman/Review of Palaeobotany andPalynology 90 (1996) 223-247

A CO CO LU

ECONOMIC REPRODUCTIVE DISPLACIVE REPULSIVE Fig. 6. Four phases of establishment of a new Uneage. Once the genetically novel propagule (asterisked) germinates, its individual survival requires only economic establishment. However, lineage establishment necessitates reproduction and population expansion. Any current occupants of the preferred niche must be displaced, and the novel lineage must then resist attempted invasions from other prospective occupants of the niche. Note that (1) botanical "competition" can only be indirect and mediated via differential utilization of the same resources, and (2) the displacive phase of establishment requires a higher level of fitness than the repulsive phase ("home-field advantage" sensu Pimm, 1984, 1991). EstabUshment of low-fitness "hopeful monsters" therefore requires a vacant niche. (See also Bateman and DiMichele, 1994a.)

DiMichele et al., 1992). The dominant dynamics ing structural variability during the Early and in these kinds of ecosystems would have been Middle Devonian, when swamp and periswamp location and occupation of space. This was essen- floras were already ecologically distinct (e.g. Tasch, tially an r-selected world. At this stage, the system 1957; Edwards, 1980; Gensel, 1987; Bateman, should have been highly invadable from both 1991; DiMichele et al., 1992). Thus, at this early ecological and evolutionary perspectives, due to stage in land plant history, ecology is less a con- the lack of integrated, multispecies communities straint than a reflection of the progress of pheno- on Early Devonian landscapes. Competition for typic evolution. When organisms began to evolve space rather than light or nutrients should have structural and physiological attributes that permit- permitted new species to invade and estabUsh on ted them to escape the wetter landscapes, or to undersaturated landscapes with few mutualistic exploit those landscapes more fully, they encoun- interactions among species (cf. Fig. 6). In current tered little counter-selection from existing occu- "ecojargon", the Early Devonian was a time of pants (cf. Fig. 6). In such a scenario, physical low connectance (plants had few coevolved inter- tolerance predominates over biotic interaction in actions and interdependencies), high resilience dictating evolutionary pattern. This is fully consis- (following disturbances, ecosystems were able to tent with the evolutionary model developed by return to rapidly to the starting condition), and Valentine (1980) and elaborated by Erwin et al. low resistance (ecosystems were easily invaded by (1987). species new to the area or newly evolved) (see Pimm, 1984). The long lag times in the develop- 3.4. Ecological limits to the radiation ment of ecological structure reflect natural lags in the evolutionary process; unlike today, in the Early Why did the radiation of vascular plants stop Devonian there simply were no structurally com- with the three major lineages of lycopsids (homo- plex species to invade the low resistance landscapes sporous forms, selaginellaleans, and rhizomorphic of the day. forms) and three or four major trimerophyte- The distinct ecological strategies of the major derived lines (sphenopsids, progymnosperms-seed clades apparently evolved in concert with increas- plants, and one or more distinct types of ferns)? W.A. DiMichele, KM. Bateman/Review of Palaeobotany andPalynology 90 (1996) 223-247 239

Certainly, these groups do not exhibit the full increasingly well defined with distinct hierarchical spectrum of possible ways to build a vascular structure. As major class-level lineages evolved plant. The answer is probably two-fold. Phenotypic and became established they began to partition and genotypic constraints, at some level, impose the land surface and define the biotic characteris- limits on subsequent morphological change. Thus, tics of particular physical environments. These the maximum extent of phenotypic divergence per patterns then began to constrain the likelihood of clade must have decUned sharply once develop- establishment of subsequent highly divergent mentally complex body plans evolved. A morpho- forms. Thus, clades and ecological space co- logical argument of this type is difficult to test evolved; the morphological envelope and ecologi- directly due to the antiquity of the event and our cal envelope were established simultaneously inability to sample the full spectrum of variability (Fig. 4). As discussed earlier, an ecologically produced by any extinct species (as opposed to undersaturated environment favors a "novelty" the full extent of variability that survived). radiation (sensu Erwin, 1992), particularly in the Nonetheless, attempts have been made to use Paleozoic where complex morphologies and strong phylogenetics to gauge phenotypic disparity taxonomic preferences for particular ecological among Paleozoic marine invertebrates (Briggs settings had not yet evolved. The combination of et al., 1992; Foote, 1994), and similar paleobotani- available ecological resource space and relatively cal studies would vmdoubtedly yield interesting simple organisms with,weak developmental canal- results. ization enhances the survival of highly derived The second factor, again stated explicitly by morphologies, which are generally classified as the Valentine (1980), is the progressive saturation of stem lineages of higher taxa. Such radiations begin ecological resource space (Fig. 4). Most authors to slow as ecological-adaptive space is filled, which have treated ecological space as a relatively imi- selects proportionately more against progressively form background. Valentine's (1980) preferred more derived forms. As the survival of the more analogy was pre-existing tesserae on a checker- deviant phenotypes declines, ecospace is filled by board (see also DiMichele et al., 1992; Hanski, the constantly present background of less pro- 1994). Basal, highly divergent Uneages are foundly modified derivatives, which we recognize envisioned as needing disproportionately large as species within the major taxonomic groups. amounts of ecospace, due largely to weakly canal- Wetlands and terra firma landscapes formed the ized development and their consequent inability to first major ecological dichotomy within what could withstand serious competition for resources. Later- be considered the lowland tropical biome. Early evolving offshoots would need progressively wetlands were primarily the province of hetero- smaller ecospaces, within the larger initial space, sporous rhizomorphic lycopsids and possibly as their competitive abilities became less hindered some heterosporous progymnosperms (Scheckler, by weak developmental controls. Under this 1986a,b; Rex and Scott, 1987; Scott, 1988). model, ecospace is pre-existing, predefined, Although elements of other major Uneages and merely waiting for progressive occupation. occurred in such environments, the former groups Although heuristically useful, this convention is appear to have been ecologically centered there. not particularly reaUstic, especially for the early In contrast, terra fijma habitats, those with well phases of a novelty radiation into ecospace that drained to occasionally dry soils, became the prov- has no prior biotic definition. In other words, the ince of a major seed-plant radiation during the resources available to newly evolved species are Early Carboniferous (Bridge et al., 1980; Rex and not limited by the resource use patterns of pre- Scott, 1987; Scott, 1988, 1990; Bateman and Scott, existing species. 1990; Galtier and Scott, 1990). Retallack and Examination of the Late Devonian-Early Dilcher (1988) argued that during the Early Carboniferous vascular plant radiation suggests Carboniferous seed plants established the full that terrestrial landscapes were transformed from spectrum of r to AT serai strategists, with habits poorly defined with little hierarchical structure to ranging from small shrubs to large trees, in habitats 240 W.A. DiMichele, R.M. Bateman/ReviewofPalaeobotanyandPalynology90 (1996) 223-247 ranging from wet streamsides to dry soils in dis- 1990). Small stature, homosporous habit, high turbed environments. By noting this ecological reproductive output, and rhizomatous growth may dichotomy we do not mean to unply that the have permitted them to exploit such environments, evolutionary events that gave rise to the earUest where the potential for estabUshment of new species in a particular clade necessarily occurred species would have been high. in the environment (s) in which the group ulti- These floristic patterns, recognizable in the Late mately radiated. In some instances, such as that Devonian-Early Carboniferous, continued into the of the seed plants discussed in the first case study, Late Carboniferous (e.g. Scott, 1978; Pfefferkom the habitats of origin and those of ultimate ecologi- and Thomson, 1982; Phillips et al., 1985; Collinson cal success appear to be significantly different. and Scott, 1987; DiMichele and Phillips, 1994), Certainly, it has been suggested that "marginal", where such ecological differentiation has been well "disturbed", or "stressful" environments, marine docimiented both quantitatively and quaUtatively. and terrestrial, may be crucibles for major pheno- The Late Carboniferous also demonstrates the typic divergences that later estabUsh and radiate development of biomic differentiation within the in more favorable settings (e.g. Axelrod, 1967; tropical lowlands, where xeromorphic floras, con- Hickey and Doyle, 1977; Bottjer and Jablonski, sisting primarily of seed plants in general and 1988; DiMichele and Aronson, 1992). conifers in particular, existed contemporaneously Sphenopsids, especially the larger calamitean with the classic mesic-hydric biome that has long species, were centered in aggradational environ- typifed the "coal age" in paleobotany texts (Scott ments such as stream- and lake-sides, later occupy- and Chaloner, 1983; Lyons and Darrah, 1989). ing parts of peat- and clastic swamps (Scheckler, Conifer-rich xeromorphic floras appeared first in 1986b). This is a narrow subset of the broader subtropical latitudes during the early Late enviroimiental spectrum. Calamitean sphenopsids Carboniferous, subsequently migrating southward were the only major woody tree group in into the tropics (e.g. Zhou, 1994). This observation the Devono-Carboniferous with clonal, rhizoma- gives credence to the suggestion of Knoll and tous reproduction (Tiffney and Niklas, 1985). Niklas (1987) that vascular plants colonized most Examples of calamite burial and recovery growth of the the physiographic regions of the land surface are common in Late Carboniferous clastic early in their radiation. sequences (Gastaldo, 1992); this ability may have The radiation of major groups was not accompa- been the key to their success m aggradational nied by a significant increase in alpha-diversity habitats, where equisetaleans (albeit herbaceous) (diversity within individual habitats). Bateman remain common today. (1991) critically re-examined the primary literature The ferns appear to have been a diverse (and on Late Paleozoic floras, focusing on the Early probably polyphyletic) group that occupied a wide Carboniferous of northern England and southern range of environments, from wet swampy settings Scotland. By attempting to hold fades constant (Rhacophyton, zygopterids; Scott and Galtier, to avoid pooling richness measurements from 1985; Scheckler, 1986a; Scott and Rex, 1987) to different kinds of habitats, and by emphasizing fire and flood disturbed environments (Scott and potential whole-plant species, he inferred that Galtier, 1985; Scott and Rex, 1987; Scott, 1988). species richness remained relatively low through Monodominant stands were common in the Early the class-level radiation, averaging eight species Carboniferous, both in wet and dry sites, and per assemblage and perhaps as few as four per fusinization (charcoal preservation) is common. strictly delimited uniform habitat. However, This suggests that ferns radiated in disturbed envi- species in each habitat differed greatly, both phylo- ronments where habitat disruption favored plants genetically and ecologically. This interpretation is that could colonize and reproduce rapidly, and consistent with Erwin's (1992) characterization of spread to new disturbed sites before suffering a novelty radiation, in which speciation rates are extirpation (Scott et al., 1984; Scott and Galtier, low but phenotypic divergence rates are high. 1985; Rex and Scott, 1987; Bateman and Scott, Local habitats evidently remained relatively species W.A. DiMichele, R.M. Bateman/ReviewofPalaeobotanyandPalynology90 (1996) 223-247 241 poor, but major lineages occupied ecologically evolutionary events. "Home-field advantage" distinct parts of the landscape. appears to operate at the level of population dynamics, but its effects are manifested most strongly at the levels of community organization 4. Conclusions and landscape partitioning by major clades. (4) Resource partitioning within communities The Devono-Carboniferous radiation of vascu- increased, following the increase in the diversity lar plants reveals patterns and processes operating of life habits and life histories. All landscapes at diiferent levels in the evolutionary and ecological included species specialized for the full spectrum hierarchy. Our chosen examples — the evolution of life histories, from short-lived, opportunistic to of heterospory and the seed habit, and the larger long-lived, site-occupying strategies. phyogenetic pattern and timing of the radiation — (5) We believe that the vascular-plant architec- reveal linkages between events happening at the tural radiation is a manifestation of "home-field populational and clade levels, at scales ranging advantage" (sensu Pinmi, 1991) on a scale much from habitats to biomes. This radiation had several greater than that observed in modem ecosystems. immediate and important consequences: The initial radiation appears to have occurred (1) The terrestrial land surface was partitioned under low competition into a landscape that was into subenvironments that conformed strongly to unoccupied or undersatiu^ated (probably by primi- the ecological centroids of the major class-level tive homosporous plants, possibly vascular s.l.) taxa. Each of the major class-level taxa dominated (Scott, 1980, 1990; Kenrick and Crane, 1991). some portion of the land surface in the Initial occupation interacted both with natural Carboniferous, generating a taxonomically egali- selection and developmental canalization. As tarian dominance-diversity spectrum unlike that organisms became more complex morphologically of any subsequent time period. Today, for example, the likelihood of further major increases in com- the world is largely dominated by seed plants, plexity declined, reducing the average phenotypic irrespective of whether one considers terra firma, distance between ancestor and descendant species aggradational, disturbed, or wetland habitats. (though this increases the potential for profound Moreoever, in most of these habitats a single evolutionary decreases in complexity, breaking phylogenetically trivial but ecologically preeminent canalization and resetting the evolutionary clock; group, the angiosperms, is dominant. Bateman, 1994, 1995). As ecological resource (2) Alpha-diversity remained low in nearly all space became increasingly saturated the likelihood Devono-Carboniferous assemblages. However, of survival of major phenotypic deviants declined, subsequent radiations in all groups elevated diver- due to progressive increase in the average intensity sities. These radiations began in the mid-Early of selection. Also, the initial long-phase radiation Carboniferous and were largely complete by the occurred in a near-vaccuum; the potential niches mid-Late Carboniferous in the humid lowlands, had never been occupied (primary vacancy). though in the drier uplands they appear to have However, as increasingly inhospitable habitats continued into the Mesozoic. were colonized, the only opportimities lay in the (3) Radiations at lower taxonomic levels secondarily vacant niches that resulted from extrin- remained confined, for the most part, to subcom- sic environmental perturbations. Thus, large evolu- partments of the landscape. In the case of hetero- tionary jumps simultaneously became increasingly spory, for example, the earUest plants with this life less hkely to occur and much less likely to survive history successfully occupied wetlands and if they did occur (Valentine, 1980; Erwin et al., remained the dominant elements in these habitats 1987; Bateman and DiMichele, 1994a). until major extrinsically induced extinctions (6) It is always tempting to find causation at eventually permitted seed plants to occupy the the ecological level that confines a particular prob- vacated resowce space. In this way, the early lem. Our chosen examples — the origin of hetero- radiations of plants confined and directed later spory and the seed habit — may indeed have been 242 W.A. DiMichele, R.M. Bateman/Review of Palaeobotmy andPalynology 90 (1996) 223-247 mediated by strong proximate causes operating sive radiations (e.g. Briggs et al., 1992; Foote, within local ecosystems. However, study of the 1994). hierarchy of ecological organization under which The relative timing of the origin and radiation these patterns originated cautions us to consider of a clade is crucial to many of the arguments the larger context. Biotic structure and interactions advanced in this paper. Thus, the second important at levels above populations and communities may line of evidence is the date of first appearance of exert profound constraints on evolutionary a taxon (or character) in the fossil record. Given patterns. that any species will inevitably have existed prior (7) All of the key aspects of the above evolution- to its earliest detected appearance, the fossil record ary-ecological theory are at least testable indirectly offers only a minimum estunate of the absolute via the plant fossil record. Three distinct types of age of that species. Moreover, there are often paleontological data are required. severe contradictions between the relative tuning First, reconstructed fossil plant species should of appearance of taxa (1) observed in the fossil be integrated with extant species in well foun- record, and (2) predicted by the relative positions ded phylogenetic analyses (e.g. Crane, 1988; of nodes (branch points) in a cladogram Donoghue, 1989; Doyle and Donoghue, 1992; (e.g. Fisher, 1992; Norell and Novacek, 1992; Bateman and DiMichele, 1994a; Bateman, 1994, Huelsenbeck, 1994). Despite these diflSculties, rela- 1995). Including the most complete range of rele- tive timing of events can help to limit the range of vant coded taxa is unimportant for determining possible interpretations of causes and constraints, sister-group relationships and thereby classfying specifically those of the origin of a key innovation taxa on the basis of monophyly, but it is essential and the subsequent evolutionary radiation. For example, the first five origins of heterospory for the interpretation of underlymg evolutionary occurred during a relatively brief period of 20 Myr mechanisms. On average, maximizing the number in the Mid-Late Devonian (Fig. I). This suggests of coded taxa included in an analysis minunizes that several lineages that diverged during the the number of character-state transitions on each earliest (Siluro-Devonian) vascular plant radiation branch of the most parsimonious cladogram. This, crossed a vegetative complexity threshold that in turn, maximizes the probabiUty of determining allowed them to occupy aquatic-amphibious habi- the sequence of acquisition of character states tats, but the origins are insufficiently closely spaced within a lineage by distributing them on successive to suggest forcing by an extrinsic factor such as a branches of the tree (the null hypothesis must be catastrophic extinction event that freed niches for that all of the character states on a single branch reoccupation. of a cladogram were acquired together as a single The third line of evidence necessary is the envi- evolutionary event: Bateman and DiMichele, ronment of grovrth of fossil species, as inferred 1994a). during paleoecological studies. Given in situ fossils Such sequences are especially important in cases (e.g. DiMichele and Nelson, 1989; Wing et al., like heterospory, where an apparently simple life- 1992) or adequate reconstruction of transported history change affects, either directly or indirectly, fossils, much information can be gathered about an extensive range of phenotypic characters the preferred habitat (s) in which particular evolu- (Bateman and DiMichele, 1994b). It is the highly tionary radiations took place (admittedly this iterative nature of heterospory, and the apparently should not be equated with the habitat in which a broadly similar sequence of character-state acquisi- key innovation first originated, which is far more tion in each independently evolving lineage, that difficult to determine due to the low probability of most strongly implicates an underlying adaptive detection). In particular, we have argued repeat- drive (Bateman, 1995). An additional benefit of edly for the importance of home-field advantage integrated phylogenies is the ability to quantify in determining the ecological dominants of particu- morphological disparity via branch lengths, and lar habitats. Home-field advantage assumes that thus to compare the relative magnitudes of succes- the species occupying a particular niche in a partic- W.A. DiMichele, RM. Bateman/Review of Palaeobotany andPalynology 90 (1996) 223-247 243 ular habitat will resist invasion by similar pheno- evolution of form in vascular plants: a neoGoldschmidtian types (even of high fitness); this can be tested in synthesis. In: D.S. Ingram and A. Hudson (Editors), Shape and Form in Plants and Fungi. Academic, London, the fossil record if the plants are sufficiently well pp. 61-100. known and their preferred habitats have been Bateman, R.M. and DiMichele, W.A., 1994b. Heterospory: estabhshed. the most iterative key innovation in the evolutionary history of the plant kingdom. Biol. 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