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Graptoloid Diversity and Disparity Became Decoupled During the Ordovician Mass Extinction

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Graptoloid Diversity and Disparity Became Decoupled During the Ordovician Mass Extinction Graptoloid diversity and disparity became decoupled during the Ordovician mass extinction David W. Bapsta,b,1, Peter C. Bullockc, Michael J. Melchinc, H. David Sheetsd, and Charles E. Mitchellb aDepartment of the Geophysical Sciences, University of Chicago, Chicago, IL 60637; bDepartment of Geology, University at Buffalo, The State University of New York, Buffalo, NY 14260; cDepartment of Earth Sciences, St. Francis Xavier University, Antigonish, NS, Canada B2G 2W5; and dDepartment of Physics, Canisius College, Buffalo, NY 14208 Edited by Douglas H. Erwin, Smithsonian National Museum of Natural History, Washington, DC, and accepted by the Editorial Board January 19, 2012 (received for review August 31, 2011) The morphological study of extinct taxa allows for analysis of a HME (Fig. 1), they were driven to extinction during the Hir- diverse set of macroevolutionary hypotheses, including testing for nantian glaciation (7, 15). In contrast, the Neograptina simulta- change in the magnitude of morphological divergence, extinction neously speciated rapidly after the first extinction episode of the selectivity on form, and the ecological context of radiations. Late HME (15). Ordovician graptoloids experienced a phylogenetic bottleneck at The changes in morphological diversity during this interval have the Hirnantian mass extinction (∼445 Ma), when a major clade of not been studied quantitatively. Previous work suggests that only a graptoloids was driven to extinction while another clade simulta- single morphotype survived the HME (16, 17) and that the number neously radiated. In this study, we developed a dataset of 49 eco- of morphotypes recovered in the Silurian. Mitchell (18) demon- logically relevant characters for 183 species with which we tested strated that the Silurian Neograptina evolved a number of mor- i two main hypotheses: ( ) could the biased survival of one grapto- phologies that converged upon pre-Hirnantian diplograptine loid clade over another have resulted from morphological selectiv- forms. Overall, this work suggests that the Hirnantian diversi- ity alone and (ii) are the temporal patterns of morphological fication of the Neograptina was an adaptive radiation sparked by disparity and innovation during the recovery consistent with an the removal of their diplograptine competitors (7), in agreement interpretation as an adaptive radiation resulting from ecological release? We find that a general model of morphological selectivity with a common interpretation that, during recovery intervals, di- versification is driven by ecological opportunity available after a has a low probability of producing the observed pattern of taxo- – nomic selectivity. Contrary to predictions from theory on adaptive mass extinction removes competitors (19 22). Morphological data radiations and ecological speciation, changes in disparity and spe- provide a means by which to further test this hypothesis. cies richness are uncoupled. We also find that the early recovery is The protracted nature of the HME and the well-sampled fossil unexpectedly characterized by relatively low morphological dispar- record of the graptoloids allows for a high-resolution examina- ity and innovation, despite also being an interval of elevated spe- tion of processes throughout the mass extinction event. Our ciation. Because it is necessary to invoke factors other than ecology study covers ∼9 million years, divided into 10 biostratigraphic to explain the graptoloid recovery, more complex models may be zones (SI Text). In many studies of morphological disparity, 9 needed to explain recovery dynamics after mass extinctions. million years would be resolved to one or two temporal bins. The relatively high temporal resolution afforded by the graptolite graptolites | macroevolution | selection | diversification | nonadaptive radiation record provides a unique opportunity to examine macroevolu- tionary change at the scale of species durations and therefore to ass extinction events are defined by their effect on taxo- potentially recover much more detailed insights into the pro- Mnomic diversity, but they also have profound impacts on cesses of recovery from mass extinction than would otherwise the biotic diversity of morphology and ecology (1–3). Quantita- be possible. tive assessments of morphological diversity, i.e., disparity, can In this paper, we analyze the patterns and processes of dis- shed light on the selectivity of extinction and add to our un- parity change in Late Ordovician and Early Silurian Graptoloi- derstanding of the ecological context of recovery patterns after dea by using a multivariate dataset of 49 morphological extinction events (4, 5). characters for 183 species (Dataset 1). We use our data to an- In this paper, we quantify the morphological dynamics of the alyze the support for two main hypotheses. First, we use Graptoloidea during the end-Ordovician mass extinction, which resampling simulations to test whether morphological selectivity began ∼445 million years ago. This event is composed of two alone can explain the preferential survival of the Neograptina separate extinction episodes during the Hirnantian Stage (6) and during the two extinction episodes of the HME. Chen et al. (7) is commonly referred to as the Hirnantian mass extinction established that the survival and proliferation of the Neograptina (HME). These episodes of increased extinction rate are associ- during the Hirnantian cannot be explained by stochastic non- ated with the initiation and termination of a global cooling pe- fi selective processes, but it is unclear whether this pattern results riod in the rst half of the Hirnantian, during which sea-surface from selection for the relatively simple morphology of Late temperatures dropped ∼5 °C (7, 8). Graptoloids are an extinct clade of colonial zooplankton (Hemichordata) noted for their well-sampled fossil record and – Author contributions: D.W.B., M.J.M., H.D.S., and C.E.M. designed research; D.W.B., P.C.B., high rate of species turnover (9 11). Previous work on the effect M.J.M., H.D.S., and C.E.M. performed research; D.W.B., P.C.B., M.J.M., and C.E.M. collected of the HME on the Graptoloidea has revealed a tumultuous and data; D.W.B. and H.D.S. analyzed data; and D.W.B. and C.E.M. wrote the paper. complex pattern. The graptoloids experienced some of the high- The authors declare no conflict of interest. est extinction intensities among marine invertebrates during the This article is a PNAS Direct Submission. D.H.E. is a guest editor invited by the Editorial HME (12), and the surviving taxa were a limited sample of pre- Board. HME lineages. Before the mass extinction event, graptoloid lin- Data deposition: The data reported in this paper have been deposited in the Dryad re- eages can be divided into two monophyletic clades that diverged pository, http://datadryad.org/ (doi:10.5061/dryad.d24sb3h8). more than 20 million years before the HME: the Neograptina and 1To whom correspondence should be addressed. E-mail: [email protected]. the Diplograptina (13, 14). Although the Diplograptina were This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. much more species-rich and morphologically disparate before the 1073/pnas.1113870109/-/DCSupplemental. 3428–3433 | PNAS | February 28, 2012 | vol. 109 | no. 9 www.pnas.org/cgi/doi/10.1073/pnas.1113870109 Downloaded by guest on September 25, 2021 Fig. 1. Spindle diagrams and phylogenetic relationships of groups examined in this analysis, plotted through the ten graptolite biostratigraphic zones the comprise the study interval. Width of spindles corresponds to species richness per interval (scale bar at top right). Colonies of typical members of each group illustrate some of the morphologic diversity of colony forms (imaged in transmitted infrared illumination; see scale bar). Phylogenetic relationships are taken from previous cladistic analyses (13, 40). Absolute time scale for the zones is taken from Sadler et al. (39). Note that the lack of neograptine species in the uncinatus Zone reflects the rarity of normalograptid taxa in that interval rather than a poorly sampled record (45). Ordovician neograptines or unobserved variation in another set in speciation rates during the Hirnantian are the factors that of traits, such as physiological tolerances (23). resulted in the subsequent phylogenetic bottleneck of the Grap- Second, we evaluate whether the graptoloid recovery is con- toloidea. We used repeated sampling simulations to test whether sistent with the postulated model of diversification mediated by selection for neograptine-like characteristics is the only causal ecology. Under a model of adaptive radiation where ecological factor necessary to explain the Neograptina survival patterns. fi opportunity promotes diversi cation, morphological and taxo- These simulations included selective survival of neograptine-like EVOLUTION nomic diversity should correlate from interval to interval as new morphology and preserved the same extinction intensity as the two species fill the available ecospace. If the graptoloid recovery was extinction episodes (Materials and Methods). If morphological primarily driven by ecological opportunity, there should be a close selectivity is a sufficient explanation, these simulations of the ex- relationship between species richness and morphological dispar- tinction episodes should often produce computer-generated sur- ity as the neograptines diversify. Theory on adaptive radiations vivor faunas with a proportion of neograptines
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