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Dynamic Evolutionary Change in Post-Paleozoic Echinoids and the Importance of Scale When Interpreting Changes in Rates of Evolution

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Dynamic Evolutionary Change in Post-Paleozoic Echinoids and the Importance of Scale When Interpreting Changes in Rates of Evolution Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution Melanie J. Hopkinsa,1 and Andrew B. Smithb aDivision of Paleontology, American Museum of Natural History, New York, NY 10024; and bDepartment of Earth Sciences, The Natural History Museum, London SW7 5BD, United Kingdom Edited by Mike Foote, The University of Chicago, Chicago, IL, and accepted by the Editorial Board January 18, 2015 (received for review September 19, 2014) How ecological and morphological diversity accrues over geo- component of both past and present marine ecosystems (e.g., logical time has been much debated by paleobiologists. Evidence refs. 20–22). However, analysis of how this diversity arose has from the fossil record suggests that many clades reach maximal either been based on taxonomic counts (e.g., ref. 23) or has diversity early in their evolutionary history, followed by a decline adopted a morphometric approach where the requirement of a in evolutionary rates as ecological space fills or due to internal homologous set of landmarks limits taxonomic, temporal, and constraints. Here, we apply recently developed methods for esti- geographic scope (e.g., ref. 24). We use a discrete-character- mating rates of morphological evolution during the post-Paleozoic based approach and a recent taxonomically comprehensive history of a major invertebrate clade, the Echinoidea. Contrary to analysis of post-Paleozoic echinoids as our phylogenetic frame- expectation, rates of evolution were lowest during the initial phase work (25). This tree is almost entirely resolved (SI Appendix, Fig. of diversification following the Permo-Triassic mass extinction and S1) and branches may be scaled using the first appearance of increased over time. Furthermore, although several subclades show each taxon in the fossil record (SI Appendix, Table S1). We high initial rates and net decreases in rates of evolution, consistent tabulated the number of character state changes that occurred with “early bursts” of morphological diversification, at more inclu- along each branch within ∼10-million-year time intervals span- sive taxonomic levels, these bursts appear as episodic peaks. Peak ning the Permian and post-Paleozoic (SI Appendix, Table S2), rates coincided with major shifts in ecological morphology, primar- and divided this by the summed duration of branch lengths to ily associated with innovations in feeding strategies. Despite hav- compute a time series of per-lineage-million-year rates of mor- ing similar numbers of species in today’s oceans, regular echinoids phological evolution. We accounted for uncertainty in phyloge- have accrued far less morphological diversity than irregular echi- netic structure, uncertainty in the timing of the first appearance noids due to lower intrinsic rates of morphological evolution and of taxa, and uncertainty in the timing of character changes along less morphological innovation, the latter indicative of constrained each branch using a randomization approach (12). We also esti- or bounded evolution. These results indicate that rates of evolution mated rates within subclades, corroborating our findings by using are extremely heterogenous through time and their interpretation likelihoods tests to determine whether some branches had higher depends on the temporal and taxonomic scale of analysis. rates than expected given rates across the entire tree. Finally, we compared rates of evolution through time with the structure of fossil record | morphological diversification | early bursts | diversification within a character-defined morphospace, and evolutionary innovation | mode of evolution looked for evidence of differences in evolutionary modes among subclades. The pattern that emergesisoneofdynamicevolutionary ssessing how rates of morphological evolution have changed change through time: Both rates and patterns of evolution vary Aover geological time has been a major research goal of evo- lutionary paleobiologists since Westoll’s classic study of lungfish Significance evolution (1). A common pattern to emerge from the fossil record is that many clades reach maximal morphological diversity early in Biodiversification studies have often relied on constant-rate – their evolutionary history (2 4). This sort of pattern could be the models of diversification. More recently, however, there has “ ” result of an early burst of morphological diversification as taxa been an effort to identify changes in diversification rates diverge followed by a slow-down in rates as ecological space within clades. This effort has largely focused on models of becomes filled (5, 6). Internal constraint or long-term selective declining rates because many clades appear to have high initial pressures could also limit overall disparity, leading to a slowdown rates, followed by slow-downs as ecological space fills. Here in the rate of new trait acquisition over time (7, 8). However, only we provide an example of a 265 million-year-old marine in- a small proportion of fossil disparity studies have also assessed vertebrate clade where evolutionary rates show a net increase changes in rates of evolution within lineages (e.g., along phylo- over time instead. This is punctuated by intervals of high rates genetic branches) thereby providing a more nuanced understanding of morphological evolution, coinciding with major shifts in – of how this disparity came about (e.g., refs. 9 13). Simultaneously, lifestyle and the evolution of new subclades. This study dem- decreasing rates in trait evolution have been difficult to detect using onstrates the dynamic nature of evolutionary change within phylogenetic comparative data of extant taxa, because of low sta- major clades. tistical power (14, 15), loss of signal through extinction (16), and inaccuracies in reconstructing ancestral nodes (17). Here we take Author contributions: M.J.H. designed research; M.J.H. performed research; M.J.H. and advantage of recently developed methods for directly estimating A.B.S. analyzed data; and M.J.H. and A.B.S. wrote the paper. per-lineage-million-year rates of evolution from phylogenies with The authors declare no conflict of interest. both fossil and living taxa to test whether declining rates charac- This article is a PNAS Direct Submission. M.F. is a guest editor invited by the Editorial terize the evolutionary history of a major clade of marine inverte- Board. brates, the echinoids. See Commentary on page 3595. Since originating some 265 million years ago (18, 19), crown 1To whom correspondence should be addressed. Email: [email protected]. group echinoids have evolved to become ecologically and mor- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. phologically diverse in today’s oceans, and are an important 1073/pnas.1418153112/-/DCSupplemental. 3758–3763 | PNAS | March 24, 2015 | vol. 112 | no. 12 www.pnas.org/cgi/doi/10.1073/pnas.1418153112 Downloaded by guest on September 30, 2021 temporally and across subclades, such that the overall pattern Sampling biases could make rates of evolution appear elevated depends highly on the temporal and taxonomic scale of the analysis. during the Jurassic and Eocene when they have actually been SEE COMMENTARY constant through time. For example, a prior interval of poor Results and Discussion preservation or under sampling may fail to capture a significant For crown-group echinoids as a whole, rates of character change portion of taxa that originated during that period, these taxa fluctuated throughout the post-Paleozoic, but there was a net in- making their first appearance in the fossil record coincidently crease in rates overall (Fig. 1, Spearman’s Rho = 0.47, P = 0.017). only when preservation potential improves, thus creating an ar- In addition, rates more than doubled at the start of the Jurassic, tificial spike in origination. We assessed changes in the quality of exceeding preceding time intervals. Rates remained high for the the echinoid fossil record by dividing the number of lineages next 40 million years, dropping dramatically at the end of the sampled within each time interval by the number of lineages Jurassic to a rate slightly higher but still within the range of rates inferred to be present from the phylogenetic analysis (SI Ap- during the Triassic. Rates did not increase again until the Early pendix, Table S3). We found a nonsignificant correlation be- Eocene, where they again reached levels achieved in the Jurassic, tween changes in this measure of completeness and changes in and remained high for about 20 million years. Although they fall estimated rates of character change, (Spearman’s Rho = −0.24, again after the Eocene, rates are elevated to the present day P = 0.25, SI Appendix, Fig. S6). We also estimated sampling compared with rates estimated for the Triassic, and have remained intensity using the number of collections that included echinoid relatively constant since the Oligocene. Rates were at their lowest taxa sampled globally from each time interval (SI Appendix, earlier in the clade’s history, particularly during the initial recovery Table S4), and again found a nonsignificant correlation between (and putative ecological release experienced by surviving lineages) changes in sampling intensity and changes in estimated rates of ’ Rho = − P = SI Ap- following the Permo-Triassic mass extinction. The secular increase character change (Spearman s 0.29, 0.153, pendix in average rates of character change is even more apparent
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