Contrasting evolutionary flexibility in sister groups: disparity and diversity in Mesozoic atelostomate echinoids

Abstract

Temporal asymmetries in clade histories have often been studied in lower Paleozoic radiations. Post-Paleozoic patterns, however, are less well understood. In this paper, disparity and diversity changes in Mesozoic heart urchins were analyzed at the ordinal level, with contrasts among the sister groups Holasteroida and Spatangoida, their paraphyletic stem group Disasteroida the more inclusive clade, the superorder Atelostomata. A 38-dimensional landmark-based morphospace representing test architecture was used to describe morphological evolution in terms of total variance and total range. Discordances between disparity and diversity were evident and were expressed both as deceleration in morphological diversification in all groups and as disproportionately higher disparity early in the histories of the Atelostomata, Holasteroida Spatangoida. The finding that the early atelostomate disparity peak coincides with the origin of the orders Holasteroida and Spatangoida lends support to the perception of orders as semi-independent entities in the biological hierarchy and as meaningful proxies for morphological distinctness.A comparison of holasteroid and spatangoid responses to the end-Cretaceous mass extinction revealed morphological selectivity. Paleocene spatangoid survivors showed no change in disparity relative to the Campanian-Maastrichtian sample, suggesting nonselectivity. Holasteroids suffered a pronounced loss in disparity (despite a rather high Late Cretaceous level of disparity), indicating morphological selectivity of extinction.Partitioning of disparity into plastral and nonplastral components, reflecting different degrees of developmental entrenchment and functionality, suggests that the origin of holasteroids and spatangoids is more consistent with an exploration of the developmental flexibility of nonplastral constructions than with uniform ecospace occupation. Within groups, several patterns were also most consistent with intrinsic controls. For plastral landmarks, there is an apparent increase in developmental modularity and decrease in developmental constraint from disasteroids to holasteroids and spatangoids. For nonplastral landmarks, no substantial change in disparity was observed from disasteroids to holasteroids and spatangoids, suggesting the maintenance of a developmental constraint despite the passage of time and ecological differentiation. More generally, this study suggests that certain topologies of disparity and evolutionary mechanisms potentially characteristic of the lower Paleozoic radiations of higher taxa (e.g., developmental flexibility) need not be confined to any given time period or hierarchical level.

Trait-based diversification shifts reflect differential extinction among fossil taxa

“…However, stage-to-stage variation in turnover is considerable for both metazoans (39) and larger taxonomic groups (e.g., gastropods or mammals) (40)(41)(42), which means that turnover actually varies considerably over the timespans covered by the datasets that we analyze. Moreover, individual clades often have early origination rates that are much higher than extinction rates (3,(41)(42)(43)(44), which elevates DSC rather than HSC (SI Appendix, Fig. S5D).…”

“…The fossil record includes many examples of taxa possessing one set of traits losing diversity over time, whereas other taxa with different sets of traits gain diversity (1)(2)(3)(4). Similarly, phylogenies of extant taxa often suggest that speciose subclades possessing derived traits were once much less diverse than the remainder of the clade diagnosed by primitive traits (5)(6)(7).…”

“…Model 2 (elevated net speciation) posits elevated speciation rates and/or decreased extinction rates among some taxa with derived traits (11,13,14). Model 3 (elevated evolvability) posits that some characters vary only among some derived taxa and not among the remainder of the clade (3,15). These models are not mutually exclusive: elevated evolvability might elevate net speciation (models 2 and 3) (16), or elevated speciation in one part of a clade might induce elevated extinction in another part of a clade (models 1 and 2) (17).…”

Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution

“…23) or has adopted a morphometric approach where the requirement of a homologous set of landmarks limits taxonomic, temporal, and geographic scope (e.g., ref. 24). We use a discrete-characterbased approach and a recent taxonomically comprehensive analysis of post-Paleozoic echinoids as our phylogenetic framework (25).…”

Linking a Biological Mechanism to Evolvability

“…Disparity and asymmetry of species richness across monophyletic groups of organisms is an observation that has invited much explanation [1][2][3][4][5][6]. One approach to explaining this pattern has been the transformation of the concept of evolvability, from simply referring to variation available to natural selection [7] to the notion that some lineages inherently possess greater potential (because the evolution of some trait with relatively higher evolvability is not guaranteed) for speciation than other lineages [8][9][10][11].…”