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Diversity Partitioning in Phanerozoic Benthic Marine Communities

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Diversity Partitioning in Phanerozoic Benthic Marine Communities Diversity partitioning in Phanerozoic benthic marine communities Richard Hofmanna,1, Melanie Tietjea, and Martin Aberhana aMuseum für Naturkunde Berlin, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany Edited by Peter J. Wagner, University of Nebraska-Lincoln, Lincoln, NE, and accepted by Editorial Board Member Neil H. Shubin November 19, 2018 (received for review August 24, 2018) Biotic interactions such as competition, predation, and niche construc- formations harbor a pool of species that were principally able to tion are fundamental drivers of biodiversity at the local scale, yet their interact at the local and regional scale and thus can be regarded as long-term effect during earth history remains controversial. To test their the constituents of metacommunities in the geological record. role and explore potential limits to biodiversity, we determine within- Beta diversity among collections from the same formation is habitat (alpha), between-habitat (beta), and overall (gamma) diversity expected for two reasons, even though many benthic marine in- of benthic marine invertebrates for Phanerozoic geological formations. vertebrates have planktonic larval stages and thus high dispersal We show that an increase in gamma diversity is consistently generated capabilities. First, the distribution of species within a meta- by an increase in alpha diversity throughout the Phanerozoic. Beta community is predicted to be patchy (17). Even if the habitats diversity drives gamma diversity only at early stages of diversifica- represented by a formation were homogeneous, local differences tion but remains stationary once a certain gamma level is reached. This mode is prevalent during early- to mid-Paleozoic periods, in species distributions would result in compositional differences whereas coupling of beta and gamma diversity becomes increas- among sites. Beta diversity is, thus, expected to structure gamma ingly weak toward the recent. Generally, increases in overall bio- diversity also under neutral conditions (17). Second, the forma- diversity were accomplished by adding more species to local habitats, tions analyzed herein typically capture more than just one habitat and apparently this process never reached saturation during the (SI Appendix,Fig.S2) and thereby record environmental differ- Phanerozoic. Our results provide general support for an ecological entiation. Accordingly, we expect differences in faunal composi- model in which diversification occurs in successive phases of progress- tion, and therefore beta diversity. Fossil collections are usually EARTH, ATMOSPHERIC, ing levels of biotic interactions. time-averaged, i.e., they constitute a mix of skeletal elements of AND PLANETARY SCIENCES noncontemporaneous communities as a result of taphonomic and biodiversity | biotic interactions | beta diversity | alpha diversity | sedimentological processes (18). Compared with the former live paleoecology assemblages, time averaging enhances alpha diversity and dimin- ishes beta diversity in death assemblages and fossil assemblages eciphering biodiversity patterns and their drivers for the (18–20). However, time averaging does not completely eliminate Dgeological past attracts unabated interest (1, 2) to identify original beta diversity (20) and, respective gradients in species the principal processes of diversification and the response of the composition are still conserved in death assemblages (21). biosphere to environmental perturbations (3). Species interac- tions such as competition, predation, and niche construction are Significance key to the understanding of diversity accumulation and potential saturation effects in local and regional species richness (4–6). Biotic interactions are drivers of biodiversity, yet their effects on These aspects are highly scale-dependent but might be unmasked Phanerozoic marine diversity remain elusive because they oper- by testing hypotheses at the geographic and temporal scale on ate on small spatial scales. We provide the comprehensive re- which they are expected to operate. Here, we apply the concept construction of within-community, between-community, and of diversity partitioning to the fossil record to unveil the role of overall diversity on the scale of geological formations throughout biotic controls in diversification and to examine potential limits the Phanerozoic eon to gauge the effects of biotic interactions on to local biodiversity. Introduced by Whittaker (7, 8), biodiversity biodiversity. Within-community and overall diversity are posi- can be dissected into three components known as alpha diversity tively correlated and both are practically unbounded. Between- (local species richness), beta diversity (differential diversity be- community diversity drives overall diversity only at low levels of tween localities), and gamma diversity (overall species richness overall diversity, and mostly during the early- to mid-Paleozoic. of the observed system). This concept proved useful to disen- Further increase of biodiversity is generally achieved by finer tangle patterns underlying diversification in modern biota (9, resource partitioning driven by positive species interactions. 10). Some applications of diversity partitioning in deep time exist (11, 12) but are confronted with the problem that biotic factors Author contributions: R.H. designed research; R.H. performed research; M.T. and M.A. and abiotic factors (e.g., plate configuration, changes in physi- contributed new reagents/analytic tools; R.H. and M.T. analyzed data; and R.H., M.T., and cochemical conditions) increasingly intermingle from local to M.A. wrote the paper. regional and global scales (13, 14). Apart from a few studies at Conflict of interest statement: Michael Hautmann (University of Zurich), the author of the diversification model which is herein used to link diversity trajectories to competition, has short timescales (15, 16), the structure and limits of Phanerozoic been the thesis advisor of the first author. biodiversity at the habitat scale are largely unknown. This article is a PNAS Direct Submission. P.J.W. is a guest editor invited by the We used occurrence data of noncolonial benthic marine in- Editorial Board. vertebrate species (gastropods, bivalves, trilobites, brachiopods, This open access article is distributed under Creative Commons Attribution License 4.0 and echinoderms) from the Paleobiology Database (https://pale- (CC BY). obiodb.org) to determine alpha, beta, and gamma diversity of 340 Data deposition: The data and code used for this study have been deposited in GitHub, Phanerozoic geological formations (see Materials and Methods for https://github.com/fossilrich/Diversity-Partitioning. details and SI Appendix,Fig.S1). Formations are mappable geo- 1To whom correspondence should be addressed. Email: [email protected]. logical units of mostly sedimentary rock that usually maintain a This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. more or less uniform environmental architecture during a certain 1073/pnas.1814487116/-/DCSupplemental. time span at a given place in the geological past. As such, marine Published online December 17, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1814487116 PNAS | January 2, 2019 | vol. 116 | no. 1 | 79–83 Downloaded by guest on October 1, 2021 Collectively, we therefore expect beta diversity to be conveyed by the fossil collections of the formations studied herein. Utilizing formations allows us to test the significance of bi- [species] per formation Mean alpha diversity ologically controlled diversity partitioning, particularly the role 40 of species interactions, by reducing purely abiotic effects and artifacts (e.g., provinciality, tectonic configuration, preserved 0.9 rock volume per time interval, binning of time intervals) that are known to influence global diversity estimates (22, 23). This ap- proach allows us to test the general expectations of ecological 30 diversification models that are based on positive biotic interac- tions, i.e., processes such as competition, predation, and niche 0.6 construction that promote diversity. In particular, we test the theoretical diversity partitioning model of Hautmann (24) in 20 which pathways of alpha and beta diversity were used to define three phases of diversity accumulation mediated by progressively increasing levels of positive interactions (see Discussion for de- tails). In this study, alpha is the mean number of species per 0.3 collection, beta is the mean dissimilarity between collections in 10 each stratigraphic formation, and gamma is the total species richness within each formation. Results Mean beta diversity per formation [Simpson's Metric] [Simpson's per formation Mean beta diversity The trajectories of mean alpha and mean gamma diversity in 0.0 0 formations show a largely similar course during the Phanerozoic 100 200 300 400 (SI Appendix, Fig. S3 A and B). Aside from peaks in the Silurian Mean gamma diversity per formation [species] and Permian, both diversity metrics show no pronounced trend Fig. 1. Alpha–beta–gamma-plot showing the influence of alpha (red) and until the mid-Cretaceous. Since the late Cretaceous they increase ’ on average toward the recent. Beta diversity, measured using Simpson s metric as a measure for beta diversity (blue) to generate gamma diversity of all Phanerozoic geological formations. Gray areas represent the Simpson-based multiple-site dissimilarity (25) (named as Simp- ’ ’ 95% confidence intervals of curve
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