Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies
Abstract.-Global information on Paleozoic, Mesozoic, and extant non-angiosperm leaf morphologies 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 first pattern, morphological divergence of fern and seed plant leaf morphologies, indirectly recognized as part of the Paleophytic-Mesophytic transition, likely reflects reproductive and ecological divergence. The leaf-borne reproductive structures that are common to the ferns and Paleozoic seed plants may promote leaf morphological 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 morphological 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 distribution of angiosperm-like leaf traits among fossil and extant plants suggests that these traits preferentially evolve in herbaceous to understory plants of warm, humid environments, thus supporting inferences concerning angiosperm origins based upon the ecophysiology of basal extant taxa.
During the Late Devonian and Early Carboniferous, at least four vascular plant line-ages (seed plants, progymnosperms, ferns, and sphenopsids) independently evolved laminate leaves and followed the same early sequence of morphological evolution. After this initial radiation, the ferns and seed plants shared nearly the complete morphological range found in Paleozoic leaves (Boyce and KNoLinkList 2002). This repeated pattern of early evolution suggests a highly constrained radiation; however, this early history of morphological evolution contrasts strongly with the modern world dominated by angiosperms with leaf morphologies radically different from nearly all Paleozoic forms. Morphologies reminiscent of the Paleozoic do persist, but primarily only among ferns.
Living plants provide a developmental context for this evolutionary history. Marginal growth is found in fern laminae (Pray 1960, 1962; Zurakowski and Gifford 1988) that have one or two orders of veins with strictly marginal vein endings. A causal link between these morphological and developmental traits is consistent with current understanding of vascular differentiation along gradients of the hormone auxin produced in growing areas (e.g., Sachs 1991; Berleth et al. 2000). Alternatives to strictly marginal growth, including cell divisions dispersed throughout the leaf, are found in angiosperm leaves (Pray 1955; Poethig and Sussex 1985a,b; Hagemann and Gleissberg 1996; Dolan and Poethig 1998) that have many orders of veins and dispersed internal vein endings. These correlates have been used to interpret the fossil record of morphological evolution as reflecting the independent evolution of marginal meristematic growth in multiple lineages in the Paleozoic and the evolution of departures from strictly marginal leaf growth, notably in the angiosperm lineage, which dominates modern floras (Boyce and KNoLinkList 2002).
Issues regarding this transition remain unresolved. First, the distinct morphological and developmental characteristics of angiosperm leaves have factored in several theories concerning the environmental and ecological origins of the group, but rarely have they been considered as part of the broader history of leaf evolution. Second, most morphologies related to strictly marginal growth are now associated only with ferns. This loss of seed plant morphological diversity may either simply reflect the depauperate nature of the extant gymnosperm flora-and thereby perhaps be tied to the rise of an alternative form of morphological diversity among angio-sperms-or reflect an evolutionary trend independent of the decline in gymnosperm diversity.
Analysis of Morphological Diversity in the Leaves of Fossil and Extant Plants
Leaf morphologies of extant plants and Paleozoic and Mesozoic fossils were surveyed at the generic level for 19 discrete characters describing the lamina and venation (see Appendices 1, 2, and 3 for character list, references, and morphological data and ranges). This data set consists of 281 fossil and 185 extant genera. Of the fossil genera, 107 are seed plants, 60 are ferns, seven are progymnosperms, four are sphenopsids, and 103 are of other or unknown affinities. Of the extant genera, 168 are ferns and 17 are seed plants. Occurrence data were assigned to geologic epoch or period, on the basis of durations stated in taxonomic descriptions and expanded by occurrence information reported from individual localities.