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Patterns of Segregation and Convergence in the Evolution of Fern and Seed Plant Leaf Morphologies

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Patterns of Segregation and Convergence in the Evolution of Fern and Seed Plant Leaf Morphologies Paleobiology, 31(1), 2005, pp. 117±140 Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies C. Kevin Boyce Abstract.ÐGlobal information on Paleozoic, Mesozoic, and extant non-angiosperm leaf morphol- ogies has been gathered to investigate morphological diversity in leaves 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 plants after sharing the complete Paleozoic range of such morphologies with ferns and (2) the repeated evolution of more complex, angiosperm-like leaf traits among both ferns and seed plants. With regard to the ®rst pattern, morphological divergence of fern and seed plant leaf morphologies, indirectly recognized as part of the Paleophytic-Meso- phytic transition, likely re¯ects 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 specializationÐand thereby mor- phological simpli®cationÐas 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 fossil and extant plants suggests that these traits pref- erentially evolve in herbaceous to understory 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 Biology, 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 Devonian and Early Car- ginal vein endings. A causal link between boniferous, at least four vascular plant line- these morphological and developmental traits ages (seed plants, progymnosperms, 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 re¯ecting 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 sperm lineage, which dominates modern ¯o- growth is found in fern laminae (Pray 1960, ras (Boyce and Knoll 2002). q 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 ®rst 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- ®rst 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 re¯ect the depauperate nature of the ex- variance (Fig. 3). Partitioned variance is based tant gymnosperm ¯oraÐand 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 spermsÐor re¯ect 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 fossils 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 af®nities. 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 conifers 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 ®licalean perms. All other leaf taxa with adequate de- groups (Fig. 5). Filicales include the Dipteri- scription and preservational detail were in- daceae (marking the Triassic ®rst appearance cluded. of these characteristics among ferns) and at least four lineages in the large clade encom- Results passing polypod and dryopterid ferns: Blech- This global analysis demonstrates that the naceae, Thelypteridaceae, Lomariopsidaceae/ late Paleozoic maximum of morphological di- Dryopteroideae, and Polypodiaceae/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 genus Sanmiguelia
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