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Home , Callistophytales, Caytoniales, Fern, Gigantopterid, Gymnosperm, Lyginopteridales

Paleobiology, 31(1), 2005, pp. 117–140

Patterns of segregation and convergence in the of and morphologies

C. Kevin Boyce

Abstract.—Global information on , , and extant non-angiosperm leaf morphol- ogies has been gathered to investigate morphological diversity in consistent with marginal growth and to identify likely departures from such development. Two patterns emerge from the principal coordinates analysis of this data set: (1) the loss of morphological diversity associated with marginal leaf growth among seed after sharing the complete Paleozoic range of such morphologies with and (2) the repeated evolution of more complex, angiosperm-like leaf traits among both ferns and seed plants. With regard to the first pattern, morphological divergence of fern and seed plant leaf morphologies, indirectly recognized as part of the Paleophytic-Meso- phytic transition, likely reflects reproductive and ecological divergence. The leaf-borne reproduc- tive structures that are common to the ferns and Paleozoic seed plants may promote leaf morpho- logical diversity, whereas the separation of vegetative and reproductive roles into distinct organs in later seed plant groups may have allowed greater functional specialization—and thereby mor- phological simplification—as the seed plants came to be dominated by groups originating in more arid environments. With regard to the second pattern, the environmental and ecological distri- bution of angiosperm-like leaf traits among and extant plants suggests that these traits pref- erentially evolve in herbaceous to plants of warm, humid environments, thus sup- porting inferences concerning angiosperm origins based upon the ecophysiology of basal extant taxa.

C. Kevin Boyce. Organismic and Evolutionary , Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138 Present address: Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637. E-mail: [email protected]

Accepted: 4 June 2004

Introduction 1962; Zurakowski and Gifford 1988) that have one or two orders of veins with strictly mar- During the Late and Early Car- ginal vein endings. A causal link between boniferous, at least four line- these morphological and developmental traits ages (seed plants, , ferns, is consistent with current understanding of and sphenopsids) independently evolved lam- vascular differentiation along gradients of the inate leaves and followed the same early se- hormone auxin produced in growing areas quence of morphological evolution. After this (e.g., Sachs 1991; Berleth et al. 2000). Alterna- initial radiation, the ferns and seed plants tives to strictly marginal growth, including shared nearly the complete morphological cell divisions dispersed throughout the leaf, range found in Paleozoic leaves (Boyce and are found in angiosperm leaves (Pray 1955; Knoll 2002). This repeated pattern of early Poethig and Sussex 1985a,b; Hagemann and evolution suggests a highly constrained radi- Gleissberg 1996; Dolan and Poethig 1998) that ation; however, this early history of morpho- have many orders of veins and dispersed in- logical evolution contrasts strongly with the ternal vein endings. These correlates have modern world dominated by angiosperms been used to interpret the fossil record of mor- with leaf morphologies radically different phological evolution as reflecting the indepen- from nearly all Paleozoic forms. Morphologies dent evolution of marginal meristematic reminiscent of the Paleozoic do persist, but growth in multiple lineages in the Paleozoic primarily only among ferns. and the evolution of departures from strictly Living plants provide a developmental con- marginal leaf growth, notably in the angio- text for this evolutionary history. Marginal lineage, which dominates modern flo- growth is found in fern laminae (Pray 1960, ras (Boyce and Knoll 2002).

᭧ 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3101-0008/$1.00 118 C. KEVIN BOYCE

Issues regarding this transition remain un- axes in the form of a morphospace. The first resolved. First, the distinct morphological and two PCO axes (Fig. 1) contain 55.7% of the in- developmental characteristics of angiosperm formation of the original data matrix, and the leaves have factored in several theories con- first three axes (Fig. 2) contain 74.1% as esti- cerning the environmental and ecological or- mated by the sum of their eigenvalues divided igins of the group, but rarely have they been by the sum of all eigenvalues (Foote 1995). considered as part of the broader history of PCO was supplemented by plotting of the av- leaf evolution. Second, most morphologies re- erage pairwise dissimilarity for all taxa and lated to strictly marginal growth are now as- for several groups analyzed individually, as sociated only with ferns. This loss of seed well as by plotting of the partitioned contri- plant morphological diversity may either sim- butions of individual groups to the overall ply reflect the depauperate of the ex- variance (Fig. 3). Partitioned variance is based tant flora—and thereby perhaps on the squared Euclidean distances between be tied to the rise of an alternative form of the members of a group and the overall cen- morphological diversity among angio- troid for the 123 principal coordinate axes —or reflect an evolutionary trend in- with positive eigenvalues (Foote 1993; Lupia dependent of the decline in gymnosperm di- 1999). versity. The character list was designed to describe the morphological diversity within leaves con- Analysis of Morphological Diversity in the sistent with marginal growth and to identify Leaves of Fossil and Extant Plants leaves that suggest the evolution of departures Leaf morphologies of extant plants and Pa- from marginal growth. Hence, the large mor- leozoic and Mesozoic were surveyed at phological diversity found within angio- the generic level for 19 discrete characters de- sperms would not be circumscribed with the scribing the lamina and venation (see Appen- current character list except as the evolution of dices 1, 2, and 3 for character list, references, an alternative to marginal growth. Proper in- and morphological data and ranges). This vestigation of morphological patterns within data set consists of 281 fossil and 185 extant angiosperm-like leaves would require a large genera. Of the fossil genera, 107 are seed number of characters (e.g., Hickey 1974; Leaf plants, 60 are ferns, seven are progymnos- Architecture Working Group 1999) that would perms, four are sphenopsids, and 103 are of not apply to and would obscure patterns other or unknown affinities. Of the extant gen- within leaf forms consistent with marginal era, 168 are ferns and 17 are seed plants. Oc- growth. Beyond an inadequate description of currence data were assigned to geologic epoch angiosperm morphological diversity with the or period, on the basis of durations stated in current character list, including a large num- taxonomic descriptions and expanded by oc- ber of nearly identically coded angiosperm currence information reported from individ- leaf genera to the current data set would over- ual localities. emphasize the narrow range of character The data were summarized with a principal states found within the angiosperms during coordinates analysis (PCO). The pairwise the PCO analysis and hinder investigation of comparison of all taxa was used to create a patterns within marginally organized leaves. dissimilarity matrix, the eigenvectors of (For further discussion of the sensitivities of which form the axes of the PCO after Gower such analyses, see McGhee 1999; Boyce and transformation of the matrix (Gower 1966) Knoll 2002.) The angiosperms have therefore and multiplication of each eigenvector by its been excluded. Similarly, linear leaves, such as corresponding eigenvalue (for greater detail those of the lycopods and many and see Foote 1995; Lupia 1999; Boyce and Knoll sphenopsids, would all be coded identically 2002). PCO provides a method for visualizing and were not included. The morphological large quantities of morphological information codings that angiosperms and linear leaves by geometrically summarizing as much of the would produce with this character set are ap- variability between taxa as possible on a few proximated respectively by the Gnetales and FERN AND SEED PLANT LEAF MORPHOLOGIES 119 by Czekanowskia and several progymnos- of the Marattiales, and in several filicalean perms. All other leaf taxa with adequate de- groups (Fig. 5). Filicales include the Dipteri- scription and preservational detail were in- daceae (marking the first appearance cluded. of these characteristics among ferns) and at least four lineages in the large encom- Results passing polypod and dryopterid ferns: Blech- This global analysis demonstrates that the naceae, , / late Paleozoic maximum of morphological di- Dryopteroideae, and /Grami- versity documented previously (Boyce and tidaceae. The last two lineages are large, het- Knoll 2002) among leaves consistent with erogeneous groups in which internally marginal growth largely represents the mor- directed veins likely evolved many times. phological range of such leaves in later time as Some of these characteristics also are found in well (Figs. 1, 3). This morphological range is fossils, such as the Triassic Sanmiguelia shared by the ferns and seed plants early in (Cornet 1986), of unknown or controversial af- their history but is subsequently partitioned finity (Trivett and Pigg 1996). between the two groups, with the seed plants progressively losing much of this range after The Morphological Divergence of Ferns a maximum (Figs. 1, 3). When not re- and Seed Plants duced to linear leaves, as in most conifers, After the Paleozoic, the seed plants pro- leaves are less compound (a characteristic not gressively lost leaf morphologies that persist included in the principal coordinates analy- among the ferns. This pattern corresponds, at sis); lamina attachment is often broad with least superficially, to patterns with- multiple equivalent veins entering the leaf; ve- in the two groups. Among lineages with a fos- nation is typically simplified to a single order sil record, 16 out of 24 filicalean families are without a midvein; and venation is parallel, extant, with only three lost since the Paleo- typically open, and runs a straight course end- zoic, compared with only 4 of 19 non-angio- ing at the distal margin. These characteristics sperm seed plant orders (compiled respec- are found in Cordaitales, , Cyca- tively from Collinson 1996; Taylor and Taylor dales, , and conifers including 1993). Morphological patterns therefore might those with nonlinear leaves, as well as more reflect the persistence of diverse morphologies poorly understood groups such as the Czek- among the ferns as a result of the persistence anowskiales and Vojnovskyales. Ferns rarely of basal lineages, versus progressive loss of have exhibited the morphologies typical of seed plant morphological diversity as a con- post-Paleozoic seed plants, but otherwise they sequence of the loss of higher-level groups. had occupied the morphological range of Pa- However, the evolution of leaf morphology is leozoic seed plants by the Triassic and they not sufficiently conservative for extinction to have maintained this morphological diversity be the cause of these morphological patterns. through to the present. Among extant ferns, the entire range of mor- Complex vascular characteristics that sug- phologies consistent with strictly marginal gest departures from strictly marginal leaf growth is covered by the genera of a variety of growth have evolved repeatedly, and these ve- individual families (Fig. 2A). Furthermore, nation patterns are found at low frequency at linking morphological diversity to extinction all times after their first appearance in the rates would not address the absence of ferns Permian seed plants (Fig. 4). from the morphological range to which the Other seed plants to have independently seed plants became restricted (Figs. 1A, 2B). evolved these leaf characteristics are the Tri- The leaves of several early diversifying seed assic peltasperms, as well as the angiosperms plant groups, such as the and and Gnetales with leaf macrofossil records , are as morphologically di- that begin in the . These leaf traits verse as those of the ferns, but later groups ex- occur in all three extant fern orders: in Ophiog- hibit a much more restricted range of mor- lossum of the Ophioglossales, in phologies. DiMichele and Aronson (1992) em- 120 C. KEVIN BOYCE

FIGURE 1. Principal coordinates analysis of global Paleozoic and Mesozoic fossils and extant fern and gymnosperm genera. Stratigraphic distribution of morphologies for all taxa (A) and phylogenetic distribution of morphologies for fossil and extant seed plants segregated based on Paleozoic or Mesozoic time of greatest diversity (B, C). ‘‘Ferns’’ includes Filicales, Marattiales, Ophioglossales, and . ‘‘Paleozoic pteridosperms’’ includes Lyginop- teridales, Medullosales, and . ‘‘Mesozoic pteridosperms’’ includes , Corystosper- males, and . FERN AND SEED PLANT LEAF MORPHOLOGIES 121

FIGURE 2. Phylogenetic distribution of morphologies among extant ferns (A), based on principal coordinates anal- ysis of Figure 1 plotted against a black background of all extant fern genera and among all extant (B) plants plotted against a black background of all fossils included in the analysis. (Phylogeny based on Hasebe et al. 1994 and Pryer 1995. names available in Figure 5.) phasized that drier environments foster the nation patterns and morphologies. Therefore, evolution of morphological novelty and doc- dry, peripheral environments may well have umented that many higher-level groups orig- fostered the evolution of the innovations in re- inated in drier extrabasinal settings before lat- productive morphology that are given the er moving into basinal environments as wet- most weight in establishing ordinal-level seed lands contracted late in the Paleozoic. This plant groups, but these environments appear ‘‘paleophytic/mesophytic’’ transition (re- to have fostered convergence in the evolution viewed in Knoll 1984) corresponds to the re- of leaf morphologies. This morphological con- placement seen here of seed plant groups with vergence may well be adaptive in drier envi- morphologically diverse fernlike leaves by ronments. The theoretically ideal morphology those with a more restricted range of leaf ve- for maximizing water transport efficiency 122 C. KEVIN BOYCE

FIGURE 3. A, Pairwise dissimilarity for the entire data set and for individual groups analyzed separately. B, Con- tribution of different groups to the variance of the overall data set. Seed plant subgroups are not expected to be monophyletic. Jumps in variance values between the Late Cretaceous and the Recent reflects the larger number of taxa available in the living record and the fact that all living taxa can be assigned unambiguously to ferns or seed plants, whereas a large proportion of taxa are unassignable to either group in all other time intervals.

(Givnish 1979) is approached by these seed alone. The need for greater supply of water plant groups: a leaf with a single order of and photosynthate to specific areas of straight, unbranched veins radiating from the production rather than to a more homoge- point of attachment. neous photosynthetic surface would likely re- The morphologically diverse leptosporan- sult in different optimal vein patterns. Sup- giate ferns, however, are also among the porting the mass of reproductive structures groups thought to have originated in drier, pe- may in some cases favor alternative vein pat- ripheral environments (Scott and Galtier 1985; terns as well. DiMichele and Aronson 1992). The dual role This conflict of optimizing for both photo- fern leaves typically play in both photosyn- synthetic and reproductive function might ex- thesis and might lead to a larger plain the overlap between the morphological range of morphologies than would be expect- range of the ferns and the Paleozoic pterido- ed by selection for photosynthetic function sperms, known in several cases to have borne FERN AND SEED PLANT LEAF MORPHOLOGIES 123

FIGURE 5. Phylogenetic distribution of venation char- acteristics among extant ferns. Fern families can be highly variable, and labeled taxa often include members that do not conform to the indicated morphological characteristics.

plants. This pattern is shown in full within fossils that have been interpreted as : the earliest have borne directly on leaves of taeniopterid morphologies (Mamay 1976; Gillespie and Pfefferkorn 1986; Axsmith et al. 2003), whereas Mesozoic cycads with repro- ductive organs segregated into independent

FIGURE 4. Stratigraphic distribution of basic venation structures tend towards leaf morphologies characteristics in fossil and extant leaves plotted on more typical of extant and principal coordinates analysis of Figure 1. (e.g., Triassic Leptocycas [Delevoryas and Hope 1971]). reproductive structures on the lamina of fo- Some ferns do have morphologically dis- liage leaves (medullosans [Halle 1929]; gigan- tinct fertile and nonfertile leaves. This dimor- topterids [Li and Yao 1983]; glossopterids phism often consists only of a less extensive [Surange and Maheshwari 1970; Surange and lamina of the same morphology, but can in- Chandra 1972]; others [Delevoryas and Taylor volve complete loss of the lamina in entire 1969; Galtier and Be´thoux 2002]). The mor- or portions thereof. However, the ex- phological ranges of later seed plant groups tent of dimorphism can be variable within in- would then be free to diverge from that pre- dividual genera and families and, even in the viously shared with the ferns when the re- more extreme cases, fertile and vegetative quirements of reproductive function were seg- leaves typically share the same architec- regated into separate structures in later seed ture. These distinctions suggest that much less 124 C. KEVIN BOYCE developmental and genetic divergence be- morphologies typical of mesophytic foliage. tween these forms is present than would be However, several groups likely to have leaf-in- expected with any of the modifications be- dependent reproductive structures at least tween fertile and vegetative structures exhib- partially deviate from this pattern: the peltas- ited by extant seed plants. perms, corystosperms, Caytoniales, and Pen- If seed plant lineages with and without leaf- toxylon. Although their architecture often is borne reproductive structures are considered unknown, these plants, which maintain a separately, two distinct dynamics can be rec- more diverse array of leaf morphologies, tend ognized in the overall seed plant pattern of to be smaller, subcanopy plants (Harris 1983; gradual decline following a Paleozoic high in Bose et al. 1985) for which hydraulic speciali- morphological disparity. First, seed plants zation of the leaves may have been less im- with leaf-borne reproductive structures flour- portant. Where either canopy dominance or ish in the Paleozoic before disappearing early drier, more open environments are likely in in the Mesozoic. Second, seed plants with leaf- these groups, there is a trend towards more independent reproductive structures main- mesophyte-like morphologies, e.g., Xylopteris tain a smaller, stable morphological range in the Corystosperms. Such partial approxi- throughout their history through to the pre- mations are also found among larger in sent (Fig. 3). The first appearance of this latter, lineages with leaf-borne reproductive struc- more derived is with the mid-Carbonif- tures, e.g., the glossopterids, and the largest erous Cordaitales, which had simple, strap- Medullosan trunks in the earliest Permian (re- shaped leaves with a single order of parallel, viewed in Taylor and Taylor 1993) coincident open veins running to the distal margin that with abundant Odontopteris foliage. were remarkably different from the large, pin- Evolutionary constraints are often evoked nately compound fronds with a diverse array with regard to morphological limitations (re- of pinnule venation patterns that were borne viewed in Wagner 2001), but the patterns dis- by pteridosperms. cussed here suggest that such constraints can In living seed plants, peak reproductive have unexpected outcomes. A single optimal and photosynthetic activity are typically tem- form may exist for a particular function, but porally segregated, even in the Tropics (re- optimizing for multiple functions results in viewed in Burnham 1993). Staggered sched- many coequal, suboptimal forms (Niklas ules of vegetative and reproductive organ pro- 1994). The evolution of a narrow range of leaf duction confer potentional advantages for morphologies may have been permissible in both biotic and abiotic syndromes seed plants, owing to the segregation of re- (Fenner 1998; Sakai 2001), each of which has productive and photosynthetic functions. The been inferred for different Paleozoic seed plants (Taylor and Millay 1979; Taylor 1988; ferns have always had to balance reproductive Crepet 2001). Exploitation of such advantages and vegetative leaf functions and have always would be precluded if seed and organs had a diverse range of leaf morphologies. In are borne on leaves. Furthermore, direct hy- this case, any evolutionary constraints appear draulic and energetic competition of photo- to have been acting upon the morphologically synthetic and reproductive activities may diverse group. Presumably, these later seed have made Paleozoic pteridosperms more vul- plants would be more morphologically di- nerable to fluctuations in water supply. Seg- verse, rather than less, if all of morphology regation of these processes into independent and anatomy were taken into account, instead organs may have been important for the oc- of just leaves. However, the possibility of such cupation of drier and more seasonal counterintuitive relationships between evolu- where many later seed plant groups appear to tionary constraint and its expression in the have originated. fossil record of morphological diversity Segregation of photosynthetic and repro- should be considered, because paleontologists ductive functions would allow the specializa- must always work with such partial records, tion of leaves for hydraulic supply and the regardless of study organisms. FERN AND SEED PLANT LEAF MORPHOLOGIES 125

The Repeated Evolution of Alternatives to logical transitions, such as from open to retic- Strictly Marginal Growth ulate venation, the evolution of leaves with in- ternally directed veins and nonmarginal vein Leaf venation with many orders, extensive endings has occurred at least four times in the reticulation, and vein endings dispersed seed plants and seven times among ferns. Al- throughout the leaf is often considered a hall- though these leaf morphologies are often dis- mark of the angiosperms, and the presence of tinctive and unlikely to be confused with this syndrome, or a subset of its characteris- those of angiosperms, they are all similar in tics, has been used to argue angiosperm affin- suggesting departures from the strictly mar- ity for a variety of fossil plants (e.g., Surange ginal laminar growth inferred to be the an- 1966; Melville 1969; Asama 1985; Cornet cestral condition in both ferns and seed plants 1986). These leaf characteristics have also been (Doyle and Hickey 1976; Wagner 1979; Boyce evoked as a part of several alternative hypoth- and Knoll 2002). The relatively frequent evo- eses concerning the ancestral environment lution of such characteristics suggests that and ecology of the angiosperms. Recognizing they are not an adequate indication of angio- the developmental novelty of angiosperm spermous affinity for problematic fossils with- leaves in comparison to the ancestral marginal out other lines of evidence. Also, passage leaf growth, it has been suggested that these through a nonlaminate evolutionary stage leaves represent a complete reinvention of a may be likely for the Gnetales (Doyle and laminate leaf after passage through an evolu- Hickey 1976) if linear-leaved is basal tionary phase in which the lamina was lost within the group and if they are indeed close- through adaptation to an arid, or perhaps ly related to or even nested within the conifers aquatic, environment (Doyle and Hickey (Chaw et al. 1997, 2000; Winter et al. 1999; 1976). It has also been argued that details of Bowe et al. 2000; Magallo´n and Sanderson angiosperm leaves support an herbaceous or- 2002), but the frequent evolution of these leaf igin for the group along mesic, frequently dis- characteristics among the ferns indicates that turbed stream margins (Taylor and Hickey such a scenario should not be considered nec- 1996). Other suggested advantages of differ- essary for the angiosperms. ent aspects of angiosperm leaf venation pat- Ferns represent the majority of independent terns, without necessarily making claims re- of leaf morphologies that suggest garding angiosperm origins, include in- departures from strictly marginal growth. creased structural support of a large thin lam- The center of diversity of these lineages is in ina (Givnish 1979), the maximization of predominantly shaded areas of warm wet en- photosynthetic rate with high light and nutri- vironments (compiled from Kramer and ent availability (Bond 1989), a neotenic accel- 1990), as is the case for ferns in general eration of the life cycle (Takhtajan 1976), and and the first appearance of many lineages the ensuring of an adequate water supply un- within the Filicales (Skog 2001). The Triassic der arid conditions (reviewed in Roth-Nebel- first occurrence of complex reticulation and sick et al. 2001). The obvious complication is internally directed veins within the ferns is in that hypotheses concerning the site of angio- the dipterids, known from China (Li 1995), sperm origination and the initial selective ad- which was a series of equatorial islands with vantage of various aspects of angiosperm bi- high rainfall at this time (Shangyou et al. ology are poorly constrained because angio- 1990), and from northern (Harris 1926) and sperms now dominate most terrestrial envi- southern (Retallack 1977; Anderson and An- ronments. However, any patterns of ecological derson 1985) midlatitudes, which were warm, distribution among the unrelated groups that high-rainfall zones in hothouse re- have convergently evolved angiosperm-like gimes (Wing and Sues 1992; Ziegler et al. leaves may perhaps indicate the initial ecolog- 2003). The pre-Cenozoic record of the clade in- ical conditions from which the angiosperms cluding the dryopterid and polypod ferns is radiated. controversial (Collinson 1996), and neither Though less frequent than other morpho- nor Christensenia has a fossil re- 126 C. KEVIN BOYCE cord, but the Cenozoic radiation of these lin- taceous of Brazil (Rydin et al. 2003) should eages appears to be coincident with the rise of provide a more robust understanding of the modern, angiosperm-dominated, tropical rain earlier history of the group. . The evidence presented here concerning the Fossil seed plant examples of the evolution preferential ecology and environment of ori- of more angiosperm-like leaves largely corre- gin of angiosperm-like leaf traits in non-an- spond to the conditions described for ferns; giospermous plants is consistent with several they tend to be smaller plants in warm, at least lines of evidence from the early history of the seasonally wet environments, although not al- angiosperms and their basal living members. ways likely to have been heavily shaded. Gi- The paucity of angiosperm gantopterid leaves are known from the Perm- relative to other angiosperm organs and ian of China and the southwestern United to wood suggests that the angio- States, although the two may not be closely re- sperms were not initially large trees (Wing lated (Asama 1962, 1985). The diverse Chinese and Tiffney 1987). Recent molecular phylog- material allows reconstruction of the plant as enies have converged on a phylogeny of an- a (Li and Taylor 1999) in a wet, tropical giosperms (Mathews and Donoghue 1999; (Ziegler 1990), although such lycopod- Qiu et al. 1999; Soltis et al. 1999; Barkman et dominated forests are likely to have had an al. 2000) with basal branches that consist of open canopy (DiMichele and DeMaris 1987). smaller woody plants of shaded, wet, tropical North American are found in environments that are frequent sites of distur- riparian environments that would have been bance (Feild et al. 2003a,b). In this setting, the the wettest areas in a landscape at least sea- evolution of more angiosperm-like vein pat- sonally dry (DiMichele and Hook 1992). Tri- terns may be involved in providing physical assic Sanmiguelia is found on levees in season- support (Givnish 1979) and equitable distri- ally wet environments (Ash 1987). The peltas- bution of water (Zwieniecki et al. 2002) across perms are thought to have been woody, be- the larger lamina common in shaded environ- cause of the deciduous nature of their leaves ments, perhaps also aiding in the exploitation and reproductive organs (Crane 1985). Com- of light flecks. The remarkable aspect of an- plex vascular characteristics are found in a giosperm leaves may not be so much their group of Triassic foliage taxa that have been complex morphology, as such complexity has related to the peltasperms by cuticular char- evolved repeatedly in smaller, understory acteristics and interpreted as an understory plants in warm, humid environments, but component of conifer-dominated, wet, warm rather the ability of angiosperms to export this temperate forests of mid latitude Eurasia complex morphology to so many other envi- (Dobruskina 1975, 1995). ronments. Morphological and ecological divergence within the living Gnetales hampers attempts Discussion to infer ancestral states for the group (Crane For the terrestrial biota, the Paleozoic has 1996). The living representatives with nonlin- been described as a time of ecosystem assem- ear leaves are , a liana to small in bly fundamentally different from later time tropical forests, and the plant Welwit- (DiMichele and Hook 1992), an assessment schia. In the fossil record, Drewria from the broadly mirrored by the patterns described Early Cretaceous Potomac Group of Virginia here. After the initial evolution of develop- (Crane and Upchurch 1987) had a slender mental mechanisms in Paleozoic plants, eco- stem with no evidence of or logical and architectural specializations were dormancy and the plant is reconstructed partitioned in the post-Paleozoic, including as an herbaceous to perhaps shrubby member the phylogenetic segregation of morphologies of streamside, early-successional vegetation in derived from marginal growth and the re- a mesic environment. A diverse gnetalean as- peated evolution of departures from strictly semblage, including broadleaf examples, that marginal growth. has recently been discovered in the Early Cre- A great deal of developmental diversity is FERN AND SEED PLANT LEAF MORPHOLOGIES 127 found among plants with nonmarginal leaf with those of fossils (Fig. 2B) suggests that growth (e.g., comparison of Liriodendron and many hypotheses concerning developmental Quiina in Foster 1952). For example, some fos- and physiological implications of different sil morphologies that are here lumped with leaf morphologies seen in the fossil record can diffuse growth, such as the gigantopterids Ev- be tested with study of living analogues. olsonia and Gigantopteridium, suggest a com- bination of marginal and internal growth in Acknowledgments discrete intercalary zones. Because of this di- Software for creation of the dissimilarity versity, the repeated evolutions of alternatives matrix and analysis of variance was written by to marginal growth are unlikely simply to R. Lupia (available at http://geosci.uchicago. replicate a fixed evolutionary sequence of edu/paleo/csource). B. Craft provided pro- morphologies, as was seen with the evolution gramming assistance. A. Knoll, N. M. Hol- of marginal growth during the Paleozoic brook, D. Pfister, C. Marshall, and D. Sunder- (Boyce and Knoll 2002); however, a much more lin provided helpful discussion. This work detailed analysis would be needed to deter- was supported by a National Science Foun- mine whether regularities exist. The angio- dation grant (ERA 0106816) and a National sperm leaves in the Cretaceous Potomac Research Council/NASA Astrobiology Insti- Group show a progression toward more high- tute associateship. ly organized venation and more-discrete dif- ferences between successive vein orders Literature Cited (Doyle and Hickey 1976), a pattern with which Anderson, J. M., and H. M. Anderson. 1985. Palaeoflora of other groups can be compared. Despite any southern Africa. Balkema, Rotterdam. Asama, K. 1962. Evolution of the Shansi flora and origin of the developmental diversity subsumed into the simple leaf. Science Reports of the Research Institute of To- classification of alternatives to marginal hoku University, series 2, special volume 5:247–273. growth, these leaves may be physiologically ———. 1985. 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Appendix 3 Phylogenetic af®nity, literature sources, and stratigraphic range for all taxa included in the analysis. Af®nity of fossil ferns, seed plants, progymnosperms, and sphenopsids identi®ed to the ordinal level; living ferns assigned to families. An af®nity of ``Other'' indicates unknown af®nity, known af®nity to a group not discussed here, or a form-genus of multiple af®nities. Abbreviations: C, Carboniferous; D, Devonian; E, Early; J, Jurassic; K, Cretaceous; L, Late; M, Middle; P, Permian; Tr, Triassic. 132 C. KEVIN BOYCE

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Appendix 3. Continued. 134 C. KEVIN BOYCE

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Appendix 3. Continued.