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Mass Extinctions Drove Increased Global Faunal Cosmopolitanism on the Supercontinent Pangaea

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Mass Extinctions Drove Increased Global Faunal Cosmopolitanism on the Supercontinent Pangaea ARTICLE DOI: 10.1038/s41467-017-00827-7 OPEN Mass extinctions drove increased global faunal cosmopolitanism on the supercontinent Pangaea David J. Button1,4,5, Graeme T. Lloyd 2, Martín D. Ezcurra1,3 & Richard J. Butler1 Mass extinctions have profoundly impacted the evolution of life through not only reducing taxonomic diversity but also reshaping ecosystems and biogeographic patterns. In particular, they are considered to have driven increased biogeographic cosmopolitanism, but quantita- tive tests of this hypothesis are rare and have not explicitly incorporated information on evolutionary relationships. Here we quantify faunal cosmopolitanism using a phylogenetic network approach for 891 terrestrial vertebrate species spanning the late Permian through Early Jurassic. This key interval witnessed the Permian–Triassic and Triassic–Jurassic mass extinctions, the onset of fragmentation of the supercontinent Pangaea, and the origins of dinosaurs and many modern vertebrate groups. Our results recover significant increases in global faunal cosmopolitanism following both mass extinctions, driven mainly by new, widespread taxa, leading to homogenous ‘disaster faunas’. Cosmopolitanism subsequently declines in post-recovery communities. These shared patterns in both biotic crises suggest that mass extinctions have predictable influences on animal distribution and may shed light on biodiversity loss in extant ecosystems. 1 School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. 2 School of Earth and Environment, Maths/Earth and Environment Building, The University of Leeds, Leeds LS2 9JT, UK. 3 Sección Paleontología de Vertebrados, CONICET−Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Avenida Ángel Gallardo 470, Buenos Aires C1405DJR, Argentina. 4Present address: North Carolina Museum of Natural Sciences, Raleigh, NC 27607, USA. 5Present address: Department of Biological Sciences, North Carolina State University, 3510 Thomas Hall, Campus Box 7614, Raleigh, NC 27695, USA. Correspondence and requests for materials should be addressed to D.J.B. (email: [email protected])orto R.J.B. (email: [email protected]) NATURE COMMUNICATIONS | 8: 733 | DOI: 10.1038/s41467-017-00827-7 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-017-00827-7 arth history has been punctuated by mass extinction (and sampled) within a given locality or not. It does not explicitly events1, biotic crises that fundamentally alter both incorporate information on the supra-specific phylogenetic E 1, 2 biodiversity and biogeographic patterns . A common relationships between taxa, such as could be used to estimate generalisation is that mass extinctions are followed by periods of phylogenetic distance present between different species present at – increased faunal cosmopolitanism1 4. For example, the Early different localities. As such, it may be difficult or impossible to Triassic aftermath of the Permian–Triassic mass extinction, apply to a global fossil record dominated by singletons (species the largest extinction event known5, 6, has been considered occurring at just one locality), as is common for tetrapods. as characterized by a globally homogeneous ‘disaster fauna’ Moreover, the results are potentially sensitive to systematic dominated by a small number of widely distributed and abundant variation in taxonomic practice (i.e., ‘lumping’ vs. ‘splitting’) and – taxa1, 3, 6 8. Similar patterns have been proposed for the differential temporal and spatial sampling. Consequently, it may aftermath of the mass extinction at the end of the Triassic9. be useful to consider how closely related sets of species from pairs However, explicit quantitative tests of changes in cosmopolitan- of localities are on a continuous scale. ism across mass extinctions are rare and have been limited to Here we present a modification of this network model that small geographical regions3 or have not incorporated information addresses these issues by incorporating phylogenetic information from evolutionary relationships (phylogeny)2, 3. into the calculation of BC. Rather than treating links between taxa In order to test the impact of mass extinctions on biogeo- in different geographic regions in a binary fashion, they are graphic patterns, a method for quantifying relative changes in instead inversely weighted in proportion to the phylogenetic cosmopolitanism through time is required. Sidor et al.3 proposed distance between them (Fig. 1a, c). These reweighted links are that the spatial occurrence data can be modelled as a bipartite then used to calculate phylogenetic biogeographic connectedness taxon-locality network, specifying the distribution of fossil taxa (pBC). As with BC, higher levels of pBC equate to more (e.g., species) within defined localities (e.g., geographic areas such cosmopolitan faunas, with less phylogenetic distance between sets as continents or basins). The biogeographic structure of this of species from pairs of localities. By contrast, lower values of pBC network can then be quantified. Faunal heterogeneity (or indicate greater endemism, and increased phylogenetic disparity biogeographic connectedness, BC) can be measured as the between sets of species from pairs of localities. This method was rescaled density of the network—the number of taxa actually applied using an informal supertree (Fig. 2a; Supplementary shared between localities relative to the total possible number of Note 1) and species-level occurrence data set of terrestrial taxon links between them3 (Fig. 1a, b). Higher values of BC amniotes ranging from the late Permian to late Early Jurassic equate to increased cosmopolitanism (i.e., less heterogeneity), (c. 255–175 Ma; see Supplementary Note 2). A k-means cluster whereas decreases in BC indicate increasing faunal endemism or analysis was used to group taxa into ten distinct geographical provinciality (i.e., greater heterogeneity). This approach has been regions based on their occurrence palaeocoordinates (Fig. 2b; previously applied to assess regional changes in cosmopolitanism Supplementary Note 3). The sampled interval includes the within southern Gondwana across the Permian–Triassic mass Permian–Triassic and Triassic–Jurassic mass extinction events, extinction3. Results indicated a decline in BC from the late and the origins of key terrestrial vertebrate clades such as Permian to the Middle Triassic, indicating that cosmopolitanism crocodylomorphs, dinosaurs, lepidosaurs, mammaliaforms, increased following the extinction event. However, this study did pterosaurs, and turtles9. It is of particular biogeographic interest not include the critical immediate post-extinction faunas (earliest due to the presence of the supercontinent Pangaea10, which began Triassic), and it is also unclear whether this regional signal is to break apart by the Early Jurassic. Although barriers to dispersal representative of global biogeographic trends. might be perceived as sparse on a supercontinent, numerous This network method uses only the binary presence–absence studies have suggested faunal provinciality and endemism – data—i.e., information on whether a given species was present on Pangaea, perhaps driven by climatic variation3, 9, 11 13. a KombuisiaShansiodonVinceria TetragoniasKannemeyeriaDolichuranusRechnisaurus bc Fig. 1 Schematic illustration of network biogeography methods. a Simplified phylogeny of Dicynodontia. b, c Taxon-locality networks. Localities are indicated by the large, pale brown circles, taxa are coloured as in (a). Taxa are connected by brown lines to the locality at which they occur. b Rescaled non-phylogenetic biogeographic connectedness (BC) of Sidor et al.3. A single taxon, Kannemeyeria (yellow), is present at all three localities, resulting in a link of value = 1(solid black line) between each locality. c Phylogenetic biogeographic connectedness (pBC), as proposed here. Links (grey lines) between taxa from different localities are weighted inversely to their phylogenetic relatedness. Line thickness and shade is proportional to the strength of the link (and thus inversely proportional to phylogenetic distance between the two taxa) 2 NATURE COMMUNICATIONS | 8: 733 | DOI: 10.1038/s41467-017-00827-7 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/s41467-017-00827-7 ARTICLE ab Synapsida Prom Scylacosuchus ore C i P i Ichibengops m P y t n P P I o n r r s c i o P o i r schor s r Olivie C t a Lycosuchus vanderrieti s t C i s G s r C i t o i Ch h t risterog e o d S r y t e r s e p i e h ro st r g l o o n c Euchamber r Mos Aki a a rdosuc r d Annath e r r P i u s e g tho o P y a o g T A hu e n Moschorh i i s p c n t a s hy e rosu l i a l erp gn o a n g n a r S k h d a o e l p a dnognathus par a r a i g Ic o o a g S u h s c a n nosau n e o i a x r n n s g x e chowhai r i g s at d d i a na p u Theriognat m i t t r o t n c t m n Me a ch r i i AMN h t g g lex o cep s u n Ictido a c s e i d t u doc i s u i I o i h w i i n l i i e chus par e r I cti athoi o s y Mirot h y a at o o n t ct b n v s o s t t s hoid c u I o r s s si i i s o erapsidu t u i c h rv s la st a id a o a h I u o hus c b s e u S i r r ct u e u d ss isa u g p s a h id a t d d d f u r a e s n ti g u i n u s s u c u l spl i o l n r s u u s nyamadziens co i e a h e e Hofme de l o n e e os dos h l ilp Viatk e t s a en n idosuc u Noth aw c a at g s si e osuc Icti g r g r r an s rus ve r l a i i i i u s e y u h s i u i s nburgensis d ri h s i s a amps n i s l u p b HF s u SAM− ur sv hu n i d e n r e es brevidens de s r ic n K n n t l g e n p i n e s i sia mirabi v e n i i s h toma hembu r v r ic u m n i u Tra o sc SAM i so i s Sca u nus sparv ss a r hus s e g a u e d ap l p d u a a l .
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