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

How ecological and morphological diversity accrues over geological time has been much debated by paleobiologists. Evidence from the fossil record suggests that many clades reach maximal diversity early in their evolutionary history, followed by a decline in evolutionary rates as ecological space fills or due to internal constraints. Here, we apply recently developed methods for estimating rates of morphological evolution during the post-Paleozoic history of a major invertebrate clade, the Echinoidea. Contrary to expectation, rates of evolution were lowest during the initial phase of diversification following the Permo-Triassic mass extinction and increased over time. Furthermore, although several subclades show high initial rates and net decreases in rates of evolution, consistent with “early bursts” of morphological diversification, at more inclusive taxonomic levels, these bursts appear as episodic peaks. Peak rates coincided with major shifts in ecological morphology, primarily associated with innovations in feeding strategies. Despite having similar numbers of species in today’s oceans, regular echinoids have accrued far less morphological diversity than irregular echinoids due to lower intrinsic rates of morphological evolution and less morphological innovation, the latter indicative of constrained or bounded evolution. These results indicate that rates of evolution are extremely heterogenous through time and their interpretation depends on the temporal and taxonomic scale of analysis.Assessing how rates of morphological evolution have changed over geological time has been a major research goal of evolutionary paleobiologists since Westoll’s classic study of lungfish evolution (1). A common pattern to emerge from the fossil record is that many clades reach maximal morphological diversity early in their evolutionary history (2–4). This sort of pattern could be the result of an “early burst” of morphological diversification as taxa diverge followed by a slow-down in rates as ecological space becomes filled (5, 6). Internal constraint or long-term selective pressures could also limit overall disparity, leading to a slowdown in the rate of new trait acquisition over time (7, 8). However, only a small proportion of fossil disparity studies have also assessed changes in rates of evolution within lineages (e.g., along phylogenetic branches) thereby providing a more nuanced understanding of how this disparity came about (e.g., refs. 9–13). Simultaneously, decreasing rates in trait evolution have been difficult to detect using phylogenetic comparative data of extant taxa, because of low statistical power (14, 15), loss of signal through extinction (16), and inaccuracies in reconstructing ancestral nodes (17). Here we take advantage of recently developed methods for directly estimating per-lineage-million-year rates of evolution from phylogenies with both fossil and living taxa to test whether declining rates characterize the evolutionary history of a major clade of marine invertebrates, the echinoids.Since originating some 265 million years ago (18, 19), crown group echinoids have evolved to become ecologically and morphologically diverse in today’s oceans, and are an important component of both past and present marine ecosystems (e.g., refs. 20–22). However, analysis of how this diversity arose has either been based on taxonomic counts (e.g., ref. 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-character-based approach and a recent taxonomically comprehensive analysis of post-Paleozoic echinoids as our phylogenetic framework (25). This tree is almost entirely resolved (SI Appendix, Fig. S1) and branches may be scaled using the first appearance of each taxon in the fossil record (SI Appendix, Table S1). We tabulated the number of character state changes that occurred along each branch within ∼10-million-year time intervals spanning the Permian and post-Paleozoic (SI Appendix, Table S2), and divided this by the summed duration of branch lengths to compute a time series of per-lineage-million-year rates of morphological evolution. We accounted for uncertainty in phylogenetic structure, uncertainty in the timing of the first appearance of taxa, and uncertainty in the timing of character changes along each branch using a randomization approach (12). We also estimated rates within subclades, corroborating our findings by using likelihoods tests to determine whether some branches had higher rates than expected given rates across the entire tree. Finally, we compared rates of evolution through time with the structure of diversification within a character-defined morphospace, and looked for evidence of differences in evolutionary modes among subclades. The pattern that emerges is one of dynamic evolutionary change through time: Both rates and patterns of evolution vary temporally and across subclades, such that the overall pattern depends highly on the temporal and taxonomic scale of the analysis.