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Physical and Environmental Drivers of Paleozoic Tetrapod Dispersal Across Pangaea

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Physical and Environmental Drivers of Paleozoic Tetrapod Dispersal Across Pangaea ARTICLE https://doi.org/10.1038/s41467-018-07623-x OPEN Physical and environmental drivers of Paleozoic tetrapod dispersal across Pangaea Neil Brocklehurst1,2, Emma M. Dunne3, Daniel D. Cashmore3 &Jӧrg Frӧbisch2,4 The Carboniferous and Permian were crucial intervals in the establishment of terrestrial ecosystems, which occurred alongside substantial environmental and climate changes throughout the globe, as well as the final assembly of the supercontinent of Pangaea. The fl 1234567890():,; in uence of these changes on tetrapod biogeography is highly contentious, with some authors suggesting a cosmopolitan fauna resulting from a lack of barriers, and some iden- tifying provincialism. Here we carry out a detailed historical biogeographic analysis of late Paleozoic tetrapods to study the patterns of dispersal and vicariance. A likelihood-based approach to infer ancestral areas is combined with stochastic mapping to assess rates of vicariance and dispersal. Both the late Carboniferous and the end-Guadalupian are char- acterised by a decrease in dispersal and a vicariance peak in amniotes and amphibians. The first of these shifts is attributed to orogenic activity, the second to increasing climate heterogeneity. 1 Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK. 2 Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, 10115 Berlin, Germany. 3 School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham B15 2TT, UK. 4 Institut für Biologie, Humboldt-Universität zu Berlin, Invalidenstraße 42, Berlin 10115, Germany. Correspondence and requests for materials should be addressed to N.B. (email: [email protected]) NATURE COMMUNICATIONS | (2018) 9:5216 | https://doi.org/10.1038/s41467-018-07623-x | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-018-07623-x major transition in the history of terrestrial faunas incorporating null model generation, is used to infer rates of occurred during the late Paleozoic. During the Carboni- dispersal and vicariance through time. Increases in vicariance A fi ferous, the tetrapod lineage diversi ed and evolved a fully and decreases in dispersal rates are found in the late Carboni- terrestrial lifestyle with the appearance of the amniotic egg1. ferous and the end-Guadalupian. The first of these shifts is During the Permian, terrestrial ecosystems developed a more attributed to the orogenic activity, the second to increasing modern trophic structure, with large numbers of terrestrial her- climate heterogeneity. bivorous vertebrates supporting a small number of macro- carnivores2. These changes occurred alongside substantial envir- Results and Discussion onmental and climate changes throughout the globe. Dispersal and vicariance rates During the Carboniferous, the assembly of the supercontinent . Throughout most of the Carbo- Pangaea was completed. With all continents connected into a niferous, vicariance rates remain low and relatively constant, single landmass, it has often been suggested that there were few aside from a slight peak in the Serpukovian (Fig. 1). The largest barriers to dispersal, producing a strongly cosmopolitan fauna, at peak in vicariance through the Carboniferous is towards the end, least at the family-level2–11. Even though in more recent years during the Kasimovian. While vicariance rates do fall after this, provincialism and faunal variation according to palaeolatitude they rise again during the middle Permian, reaching a peak in has been identified12–21 there has been very little study into the Capitanian. Both of these two peaks are followed by declines the historical biogeography of terrestrial vertebrates during the in dispersal rate (Fig. 1). Paleozoic. The Carboniferous peak in vicariance rate and decline in Many discussions of patterns of dispersal and vicariance in dispersal is most pronounced in amphibians (Fig. 2) and in Paleozoic tetrapods are short notes embedded in studies whose particular lepospondyls. The vicariance peak in amniotes is primary focus is anatomical descriptions of species22–25. Such relatively small (Fig. 3). Amniote dispersal rates fall at this time, discussions lack the application of quantitative methods and but they soon recover, unlike those of amphibians which remain instead are limited to visual examinations of a phylogenetic tree, below 0 for the rest of the Permian (Fig. 2) often just presenting the biogeographic area of the basalmost Tetrapod dispersal rates recover throughout the early Permian, member of a particular clade as the place of origin of that clade. reaching a peak during the early Capitanian (Fig. 1). The late These hypotheses are problematic, because (1) they only take into Capitanian vicariance peak, and the trough in dispersal that follows, is visible in all amniote clades and also the temnospon- account one lineage, (2) they assume a narrow ancestral area, (3) – they assume dispersal as the driving force behind the distribution dyls (Figs. 6 7). Only one lepospondyl is present by this time patterns in clades, making no allowance for vicariance and or the (Diplocaulus minimus from Morocco), so vicariance is obviously possibility of climatic barriers separating populations within a not possible in this clade. species and (4) they are at risk of changes in interpretation every time a new, more basal taxon is discovered. Late Carboniferous dispersal patterns. The dispersal and A global study of cosmopolitanism, vicariance and dispersal vicariance patterns of amphibians and amniotes indicate differing within the united supercontinent of Pangaea is integral to the responses to the geological and climate changes occurring understanding of early amniote evolution and diversification, during the latter half of the Paleozoic. For much of the Carbo- providing vital information on the impact of physical and cli- niferous, the tropical regions were covered by the coal forests, a matic barriers on different clades evolving within a single land- dense belt of tropical rainforests26. The general climate trend mass. Quantitative methods, particularly event-based methods throughout the Permian was towards warming and drying27–30, incorporating phylogenetic hypotheses, will provide a more rig- albeit punctuated by wet phases relating to the waxing and orous analysis of these issues than has previously been applied to waning of the Gondwana ice sheet31. Gradually, the substantial Paleozoic tetrapods. polar icecap present since the Devonian disappeared, the tropical Here, we present an examination of the patterns of dispersal belt across the equator narrowed, and the arid zones surrounding and vicariance of tetrapods across Pangaea during the Carboni- it expanded28,29. ferous and Permian. A supertree of Carboniferous-Permian tet- At the end of the Carboniferous, during the Moscovian stage, rapods was generated and subjected to likelihood-based the rainforest collapse is thought to have occurred: the coal biogeographic modelling analysis in order to infer the ancestral forests covering the equatorial regions were reduced to islands of ranges of internal nodes. A stochastic mapping approach, rainforest in intramontane basins of the Variscan mountains26 2 3 Dispersal Vicariance 1 2 0 –1 1 Dispersal rate Vicariance rate –2 –3 0 Art Vis Ass Sak Cap Gzh Tour Kasi Serp Bash Kung Word Mosc Chan Road Wuch Carboniferous Permian 350 340 330 320 310 300 290 280 270 260 Fig. 1 Dispersal and vicariance rates of all Tetrapoda through time. Solid grey lines represent vicariance. Dashed black lines represent dispersal. Thick lines represent the mean of the rates obtained from each stochastic mapping iteration. The thinner lines represent a standard error above and below 2 NATURE COMMUNICATIONS | (2018) 9:5216 | https://doi.org/10.1038/s41467-018-07623-x | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-018-07623-x ARTICLE a 0.5 1.5 Dispersal Vicariance 0 1 0.5 –0.5 Dispersal rate Vicariance rate 0 –1 b 0.4 0.6 0.4 0 Dispersal rate 0.2 Vicariance rate –0.4 0 c 0.2 0.8 0 0.4 –0.2 Dispersal rate Vicariance rate 0 –0.4 Art Vis Ass Sak Cap Gzh Tour Kasi Serp Bash Kung Word Mosc Chan Road Wuch Carboniferous Permian 350 340 330 320 310 300 290 280 270 260 Fig. 2 Dispersal and vicariance rates of amphibian clades through time. a All amphibians; b Temnospondyli; c Lepospondyli. Solid grey lines represent vicariance. Dashed black lines represent dispersal. Thick lines represent the mean of the rates obtained from each stochastic mapping iteration. The thinner lines represent a standard error above and below. Silhouettes from phylopic.org. b Eryops, by Dmitry Bogdanov (vectorized by T. Michael Keesey), available under Creative Commons Attribution-ShareAlike 3.0 Unported license. c Diplocaulus, by Gareth Monger, available under Creative Commons Attribution 3.0 Unported license surrounded by more arid habitats32,33. This was accompanied they observed that amniotes were less severely affected by the by a period of mass extinction among plants34,35 and a shift environmental changes at this time, a result they attributed to the from a lycopsid-dominated flora to a fern-dominated flora26. The amniotic egg and the impermeable skin giving them indepen- transition does not appear to have occurred at a consistent dence from water36. rate across the equatorial latitudes, with macrofloral and The dispersal patterns of amniotes and amphibians identified palynological
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