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https://doi.org/10.1038/s41467-018-07623-x OPEN Physical and environmental drivers of dispersal across

Neil Brocklehurst1,2, Emma M. Dunne3, Daniel D. Cashmore3 &Jӧrg Frӧbisch2,4

The and were crucial intervals in the establishment of terrestrial , 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 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 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- are char- acterised by a decrease in dispersal and a vicariance peak in and . 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 - und Biodiversitätsforschung, Invalidenstraße 43, 10115 Berlin, . 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])

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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 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 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 during the . 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 . 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). 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 , 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 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 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 ( minimus from ), so vicariance is obviously possibility of climatic barriers separating populations within a not possible in this clade. and (4) they are at risk of changes in interpretation every time a new, more 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 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 ice sheet31. Gradually, the substantial Paleozoic tetrapods. polar icecap present since the 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 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 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

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–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

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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 clades through time. a All amphibians; b ; c . 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 , 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 among plants34,35 and a shift environmental changes at this time, a result they attributed to the from a lycopsid-dominated flora to a -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 evidence suggesting coal development continued by this study might appear to support the conclusions of Sahney into the earliest Kasimovian in American localities26, but after et al.36. Both amphibians and amniotes exhibit a fall in dispersal this the last remnants of the lycopsid-dominated flora dis- rate and a peak in vicariance rate during the latest Carboniferous. appeared. Cleal et al.26, after thoroughly reviewing the sedimen- The differing patterns observed in amphibians and amniotes tological and palaeobotanical changes across Moscovian and are also supported here. The reduction of dispersal rate in Kasimovian Euramerica, suggested that increased tectonic activity amphibians is more substantial, indicating a greater sensitivity to in the Variscan orogeny altered drainage patterns in Euramerica, the changing climate. Moreover, although the aridification trends creating conditions less suitable for the lycopsid flora and driving continued throughout the Permian28,31,37, the dispersal rates of the disappearance of the coal swamps. amniotes recovered while those of amphibians remained low. The family-level diversity curves of Sahney et al.36 indicated an It might appear that amniotes were more efficient at dispersal in increase in faunal provinciality following the Moscovian, which the drier, more open habitat than the amphibians. they attributed to the rainforest collapse. It was suggested that the Before assuming that the results of this study emphatically habitat fragmentation (the separation of the coal swamps into support the conclusions of Sahney et al.36, two caveats must be rainforest islands) was responsible. In support of this hypothesis, noted. First, it is not entirely clear to what extent the two are

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0 –0.5 –1 –0.2 Art Vis Art Ass Vis Sak Gzh Cap Tour Kasi Ass Sak Gzh Cap Serp Tour Kasi Bash Kung Word Mosc Chan Road Serp Wuch Bash Kung Word Mosc Chan Road Wuch Carboniferous Permian Carboniferous Permian 360 350 340 360 350 340 330 320 310 300 290 280 270 260 330 320 310 300 290 280 270 260 Fig. 3 Dispersal and vicariance rates of amniote clades through time. a All Amniota; b Synapsida; c ; d . 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 , by Dmitry Bogdanov, available under Creative Commons Attribution-ShareAlike 3.0 Unported license. c , by Chris Jennings (vectorized by A. Verrière), available under Public Domain Dedication 1.0 license. d Concordia, by Steven Blackwood, available under Creative Commons Attribution-ShareAlike 3.0 Unported license directly comparable, since they are examining biogeography at and mountain-building was occurring, creating further barriers40. different scales; Sahney et al.36 were comparing the degree of These include the Uralides between Eastern and Asia, endemism between formations and basins, while the results and the Appalachides between North and . presented here illustrate dispersal patterns between continental- A serious issue requiring discussion is the conflict between the scale areas. Thus, our results do not provide any information on results presented here and those found by Dunne et al.41. The the habitat fragmentation model put forwards by Sahney et al.36, latter employed a networking approach to assess the biogeo- but instead illustrate the development of geographic or climate graphic connectedness of localities during the Carboniferous barriers between considerably larger regions. The second caveat and , implementing a correction to account for the to note is that the model of Sahney et al.36 makes less sense when phylogenetic non-independence of the taxa. They identified an viewed in the context of the more recent data regarding the increase in biogeographic connectedness between the Carbonifer- rainforest collapse. Rather than an extended period of habitat ous and the Cisuralian, implying greater similarity of the faunas in fragmentation into the rainforest islands, detailed examination of the early Permian. This would seem to indicate increased dispersal the and pollen records indicate that the lycopsid-dominated across the boundary, the opposite signal to that observed here. coal swamps had disappeared by the earliest Kasimovian, There are a number of possible explanations for the conflicting thereafter replaced by fern-dominated, more open environ- results. One possibility might be the differing temporal resolution ments26. Therefore, the period in which we should observe the of the studies: Here, dispersal rates are calculated at the substage increased endemism at the formation level is extremely short, level, while the finest resolution at which Dunne et al.41 calculated restricted to the late Moscovian. By the Kasmovian, the habitats biogeographic connectedness was in three bins, each containing were more uniform and should not exhibit continued isolation two or three stages. However, this seems unlikely to be the cause and reduced dispersal between them. of the discrepancy. The - dispersal rates Despite these caveats, it is possible that the rainforest collapse identified here are consistently lower than those from earlier in may still have been responsible for the continental-scale results the Carboniferous, but this interval has increased biogeographic illustrated here. As mentioned above, the collapse was not connectedness in the analysis of Dunne et al.41. synchronous across the continents, rather representing a Another possible explanation is that the difference represents contraction and progressive western shift26. If the coal swamps the different selection of regional divisions. Dunne et al.41 defined disappeared in Europe prior to , there would be an their bioregions using cluster analysis of palaeocoordinates of environmental barrier between the two, potentially restricting localities, and so both North America and Europe were divided dispersal and driving vicariance. This explanation, however, does into numerous bioregions. Here, North America was divided into not resolve the second issue described in the previous paragraph: only two regions divided by the Hueco Seaway, and Western why would the reduced dispersal of amphibians continue into the Europe was treated as a single region. The larger areas employed early Permian with no environmental heterogeneity to prevent it? in this study means that dispersal between smaller subregions An alternative explanation that would mitigate this objection would not be counted. In order to test this possibility, the might be the increased tectonic activity at the Variscan orogeny BioGeoBEARS analysis was repeated, using the same regions occurring during the Moscovian. This tectonic activity caused employed by Dunne et al.41. Since their study defines new substantial uplift and terrestrial deformation, continuing into bioregions following the Carboniferous-Permian boundary, a the Permian26,38–40. This mountain-building phase would have procedure not permitted by BioGeoBEARS, the supertree was generated a substantial physical barrier between the equatorial time sliced to the end of the Carboniferous. This does not localities, restricting not only movement between Europe and preclude the possibility of assessing the different results, as Dunne North America, but also migration between Gondwana and et al. noted an increase in biogeographic connectedness during . Elsewhere during the Moscovian, further uplift the Gzhelian, which may still be tested.

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–1 Vis Gzh Kasi Tour Serp Bash Mosc Carboniferous 350 340 330 320 310 300 Fig. 4 Carboniferous dispersal rates of all Tetrapoda, using the regional divisions of Dunne et al.41. Thick lines represent the mean of the rates obtained from each stochastic mapping iteration. The thinner lines represent a standard error above and below

This last analysis provided results that were more consistent substantial extinction at this time48, but other suggestions that with those obtained by Dunne et al.41 (Fig. 4). Dispersal rates no substantial change in either diversity or floral composition were low from the Tournasian until the Serpukovian but rose occurred34,35. It seems unlikely that the lack of inferred dispersal throughout the latter stages of the Carboniferous, reaching a peak events is due to geographically restricted sampling: the Wuchia- in the Gzhelian. That this result is obtained when both North pingian and Changshingian are among the few Paleozoic time America and Europe are divided into multiple subregions bins where data is known from both palaeotemperate and indicates that different biogeographic patterns are occurring at equatorial latitudes in both Laurasia and Gondwana20. In fact, different scales. Dispersal between the smaller-scale regions these stages contain a geographically wider sample than any appears to become easier towards the end of the Carboniferous, other, with tetrapods known from all biogeographic regions although between the larger regions it becomes more difficult. under study except North America and northern South America. This supports the inference that the principal barriers to dispersal A recent study using isotope data from amniote bones from the in the late Carboniferous were the physical barriers between provides an indication of environmental changes in the continental-scale regions rather than the local environmental temperate regions during the Permian49. The late Capitanian barriers. The island-biogeography effect posited by Sahney peak in δ13C values was interpreted as an increase in water stress et al.36, with small, local islands of forest biogeographically in i.e a period of substantially reduced humidity. By isolated by open areas, is firmly rejected: dispersal between these contrast, examinations of the geology and flora of contemporary local areas increased during the Gzhelian. palaeoequatorial formations in northern and Europe found that the late Capitanian and early represented a wet phase interrupting the general trend towards aridification Late Permian dispersal patterns. While amphibian dispersal through the Permian31,50. It is possible that the contrasting trends appears to have been restricted throughout the Permian, amniote in climate change at the different latitudes restricted the dispersal increased throughout most of the Cisuralian. This has possibility of dispersal between the two. been noted previously; while the late Permian equatorial faunas contain amphibians characteristic of early Permian equatorial localities, the amniotes are more similar to those found in con- Conclusions. Past discussions of biogeographic patterns within temporary temperate regions18,20. Interestingly, the eureptiles the Paleozoic Pangaea, and the extent of dispersal or vicariance show the same increase in dispersal as is found in . This across the continent, have been hindered by the limited use of contradicts previous suggestions that (the most quantitative methodology in making historical biogeographic diverse eureptile family during the Permian) were better suited inferences. As such, there has been considerable disagreement to arid environments42. It is only in the equatorial regions that regarding the provinciality and cosmopolitanism of the tetrapod this clade is abundant during much of the Permian; they do not faunas, as well as the potential dispersal routes across Pangaea. become abundant in the temperate regions until the Lopingian20. Quantitative analysis provides evidence of the existence of However, while remaining rare in temperate regions, they were barriers to dispersal across Pangaea, and the timing of decreases no less capable of dispersal than synapsids. in dispersal rates and peaks in vicariance rate provide evidence of The first substantial decline in amniote dispersal does not their development. Two episodes of reduced dispersal are occur until the late Capitanian, coinciding with a peak in observed: in the late Carboniferous in amphibians and at the vicariance rate. No significant change is observed in amphibians end of the Guadalupian in amniotes. Both dispersal troughs (perhaps simply due to them already being highly provincial). are accompanied by vicariance peaks. Although the nature of the The causes of this sudden and massive reduction of movement new barriers must remain speculative for the present, the first in amniotes is unclear, and our understanding is hampered by shift in dispersal rate is attributed to increased mountain- the lack of information regarding climate and environmental building at that time, while the second is hypothesised to be changes at this time. Environmental upheaval perhaps linked to due to climate barriers. flood volcanism has been suggested43–45, as has relative climatic To conclude, it is important to note that historical biogeo- stability throughout the Guadalupian and Lopingian46. The graphic analyses not only provide information on the evolu- nature and extent of the changes, and particularly their effect tionary history of the group under study, but also provide an on terrestrial environments are particularly unclear45,47. Data additional line of evidence regarding broader patterns of earth’s from plants is contradictory, with some suggestion of a history. Where more usual lines of evidence regarding continental

NATURE COMMUNICATIONS | (2018) 9:5216 | https://doi.org/10.1038/s41467-018-07623-x | www.nature.com/naturecommunications 5 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-018-07623-x arrangements or the development and break down of dispersal optimal biogeographic reconstruction (area ) with the combination of routes e.g. the Pangaea B scenario, the Carthaysian Bridge as events with minimum cost. The treefitting analysis was carried out in Treefitter 1.3B166 using the heuristic a route from Gondwana to Laurasia, the relationships of the search. The event costs used are: vicariance = 0.01, sympatric = 0.01, different faunas to each other provide a vital line of evidence. extinction = 1, dispersal = 2. This cost scheme, whereby the cost of vicariance and are minimised, is designed to maximise the likelihood of finding phylogenetically conserved distribution patterns66,67. Methods Upchurch and Hunn68 recommended time slicing (analysing taxa in each time Supertree construction. The basis for the biogeographic analysis was a formal bin separately) when using co-phylogeny reconstruction to analyse biogeography supertree of early tetrapods, designed to maximise taxonomic inclusivity. The full fi since area relationships change through time as barriers break down and new list of 49 source trees, nalised in April 2017, and the criteria for their inclusion barriers develop. While these authors carried out time slicing by dropping all tips is present in Supplementary Data 1 and Supplementary Note 1, respectively. The not present in a particular time slice, we modify this method by including tips with source trees were combined using the method “Matrix Representation with Par- ” 51,52 ghost lineages (unsampled portions of the record that may be inferred from simony (MRP) . Under this method, each node in each source tree is treated as the phylogeny) extending into the time slice. The time slices tested were the a character. Taxa within a particular node in a particular source tree receive a score , , Cisuralian, Guadalupian and . An area of “1” for the relevant character, taxa outside it receive a score of “0”, and taxa not “ ” cladogram was calculated for each time slice (Supplementary Fig. 1). included in that source tree are scored as ? . The resulting matrix may be analysed The treefitting analyses were able to provide solutions to the three disputes using parsimony. The MRP matrix was generated using the programme Super- 53 54 discussed. In all area , the eastern North American region is more tree0.85b . The matrix was analysed in the Willi Hennig Society edition of TNT , closely related to that of western Europe rather than western North America. It is using the driven search at level 100. The most parsimonious trees were searched for therefore judged that the Hueco seaway as a significant barrier, while dispersal 100 times, and then a branch-and-bound search was carried out using each most fi between eastern North America and western Europe was easier. parsimonious tree previously found as a start. The nal supertree (the strict con- In none of the area cladograms does western Europe group with South America. sensus) contains 593 terminal taxa, and is available in Supplementary Data 2. A While in most of the time bins the northern South American region is found with summary version is presented in Fig. 5. Most of the terminal taxa are genera, but other Gondwanan regions, during the Mississippian it groups with western North they also include some as-yet unnamed specimens and some species-level rela- America. These results argue strongly against the Pangaea B hypothesis; there is no tionships where these have been tested. Clades which are not known from the fossil evidence of close links between the faunas of South America and Europe. record until after the Permian but have ghost lineages extending into the Paleozoic Finally, there is strong evidence that the Cathaysian bridge has provided a link were kept in the tree during time calibration but were dropped during the bio- between the faunas of Gondwana and Laurasia. This is contra the suggestion of geographic analyses. Cisneros et al.11, who argued that, since no Paleozoic tetrapod have been The supertree was time calibrated using the method of Lloyd et al.55. This 56 found in the regions of East Asia which then formed the Cathaysian Archipelago method was itself based on an approach by Hedman , whereby the observed age of (South and Korea), tetrapod dispersal between Gondwana and Laurasia took a node relative to its successive outgroups could be used to make inferences about place via western Pangaea. However, in all area cladograms with the exception of sampling, and thereby assess how far back in time the node should be extended. the Lopingian time slice, East Asia is found to group more closely with Gondwanan Lloyd et al.55 modified this method to be applied to an entire phylogeny. The tree 57 faunas of Southern Africa than with the Eastern European fauna as argued by was time calibrated in R 3.3.2 . In order to date the root node, stratigraphically Cisneros et al.11. Thus, the lack of Paleozoic tetrapods in the Cathaysian regions is consistent outgroups were required. In this case, the Devonian tetrapods Ymeria, likely to be an artefact of preservation, and it is likely this was a frequent dispersal and Metaxygnathus were used. A maximum age constraint was placed route between the South African and Eastern European regions, at least until the on the root of 409.4 million years: the age of the split between tetrapods and fi 58 Guadalupian. The fact that in all Permian area cladograms the Eastern European lung sh inferred by a recent molecular clock study . To account for the region is found more closely related to the Gondwanan regions rather than western uncertainty surrounding the relationships and ages of taxa, 100 time calibrated Europe would suggest that the Cathaysian Bridge was actually the preferred trees were generated. For each of these, polytomies in the tree were randomly dispersal route between Gondwana and Laurasia, the Variscan Orogeny perhaps resolved and age ranges of each taxon were drawn from a uniform probability forming a more substantial barrier than suggested by Cisneros et al.11. The area- distribution covering the full possible range in which the taxon could have lived. adjacency matrix inferred from these results and used in the BioGeoBEARS The age ranges employed are shown in Supplementary Data 3. The analyses analysis is presented in Supplementary Table 2. described below are carried out on all 100 trees.

BioGeoBEARS. To infer the timing and phylogenetic position of dispersal, vicar- Founder-event . Founder-event speciation, represented in BioGeo- iance and local extinction events, ancestral geographic ranges were inferred using a BEARS as speciation events where one of the two descendant lineages of a node likelihood-based model comparison in the R package BioGeoBEARS59. The remains in the ancestral area and the other jumps to a new area59, was not functions in this package implement three different biogeographic models: DEC, permitted in the analyses in this paper. While it has been shown to be important DIVA and BayArea60,61, each of these allowing a different combination and geo- in island clades59, the model has been criticised for biasing towards cladogenetic graphic extent of biogeographic events. The phylogeny and the geographic ranges dispersal events over anagenetic69. As the model incorporates no speciation-rate of the tips were analysed using all three models, with the Akaike information parameters, cladogenetic events like founder-event speciation are assumed to take criterion used to identify the best-fitting model. This was found to be the DIVA place at fixed nodes, rather than being an outcome of a time-dependant diversi- model (Supplementary Table 1), which allows dispersal and local extinction along fication process. Anagenetic dispersal events, on the other hand, are treated as a lineages, sympatric speciation of a lineage within a single area (but not sympatric character evolving in a stochastic manner similar to the MK model, and are speciation covering multiple region), and the vicariant origin of a species over a therefore time-dependant. This difference increases the probabilities of inferring variety of range sizes. cladogenetic events such as founder-event speciation over anagentic The tetrapod-bearing formations of the Carboniferous and Permian were dispersal59,69,70. A further criticism was of the j parameter, not as a rate of founder- grouped into 13 bioregions. These were separated by a combination of physical speciation, but as a free parameter indicating the weight given to the easier mode of barriers such as mountain ranges and internal seaways, and latitudinal lines dispersal69.Afinal issue is that the founder events are also allowed to effectively intended to reflect climatic boundaries (see Supplementary Note 2 for detailed bypass the area-adjacency matrix. While this is reasonable in island clusters, it descriptions of the regions). The regions are: western North America; eastern produces unrealistic results a supercontinent where, short of circumnavigating North America, northern South America, southern South America, western the continent, the only possible dispersal routes for terrestrial are via Europe, eastern Europe, eastern Asia, northern Africa, southern Africa, adjacent areas. Madagascar, , Australia and (see Supplementary Data 4 for the areas to which each taxon was assigned). Stochastic mapping to infer dispersal and vicariance rates. The BioGeoBEARS Treefitting and the area-adjacency matrix. The biogeographic analyses carried analysis identifies the probability that a node in the phylogeny was present in a out in BioGeoBEARS incorporate a matrix indicating which areas are adjacent to particular area or combination of areas. One might infer the geographic ranges each other, thus informing the algorithm about possible dispersal routes. While the of the ancestral nodes by assuming this is represented by the most range with majority of the area-adjacency matrix could be inferred with little debate, there are the highest probability (Figs. 6–8). However, a better alternative is to use these contentious issues which will influence it, for example: (1) whether the Pangaea B probabilities to infer possible biogeographic histories via a stochastic mapping scenario, whereby North America is positioned more westerly than usually approach: drawing ancestral regions using the probabilities inferred by the Bio- depicted and western Europe is adjacent to Northern South America11,62, should be GeoBEARS analysis, and from these deducing the phylogenetic position and timing followed; (2) whether dispersal should be allowed along the Cathaysian Bridge63,64 of biogeographic events required to obtain the observed biogeographic history. between eastern Gondwana (India and Australia) and Eastern Laurasia (East Asia); For each of the 100 time calibrated phylogenies, 100 biogeographic histories (3) whether it is necessary to treat the North American provinces on either side of were generated using stochastic mapping; thus 10,000 total evolutionary histories the Hueco seaway65 as separate biogeographic regions. were tested. The timing of dispersal and vicariance events were extracted, and the In order to answer such disputes, the supertree was subjected to a treefitting number of each event in each time bin was counted. The time bins employed were analysis. This analysis uses a phylogeny and a series of event costs to calculate the informal substages, obtained by dividing each of the international stages in half. As

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Colosteidae Whatcheeriidae Baphetidae Edopoidea Temnospondyli Dvinosauria Sclerocephalidae Archegosauroidea Zatrachidae Trematopidae Micromelerpetontidae Amphibamidae Chroniosuchia

Lepospondyli Adelogyrinidae Aistopoda Captorhinidae Eureptilia Protorothyrididae Araeoscelida Tangasauridae Mesosauridae Parareptilia Lanthanosuchia Bolosauria Nyctiphruretidae Amniota Nycteroleteridae Pareiasauria Eothyrididae

Synapsida Varanopidae Edaphosauridae Tapinocephalia Anteosauridae Gorgonopsia Annomodontia Therocephalia Cynodontia

Fig. 5 Summary version of the supertree used in the analysis each bin differs in length, the event counts of each bin were divided by the length of the tree, time bins containing more nodes would exhibit a higher vicariance the bin in order to obtain a rate. count simply by chance. Therefore, for each of the 10,000 stochastic maps, The raw numbers of dispersal and vicariance events in each time bin may be a null model was also generated by simulating 100 biogeographic histories over misleading as a measure of dispersal or vicariance rate, due to the variation in the time calibrated phylogeny. A starting area/range of areas was selected at the number of lineages and nodes in each time bin (Supplementary Figs. 2–6). random from the same set of regions used in the BioGeoBEARS analysis. With If, for example, vicariance events were distributed at random across the nodes in this starting area assigned to the root node of the relevant phylogeny, the

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a 210

220

230

240 Pentaedrusaurus Phonodus Eumetabolodon dongshengensis Tichvinskia Timanophon Kitchingnathus Phaanthosaurus Theledectes Sauropareion Neoprocolophon Pintosaurus Huanghesaurus Obirkovia Shansisaurus Millerosaurus ornatus Milleropsis Bunostegos Sanchuansaurus Shihtienfenia Millerosaurus nuffieldi Nanoparia Pumiliopareia Pareiasuchus nasicornis Pareiasuchus Honania 250 d e e g i e ieeddidhiiki e a Parasaurus e i i i Scutosaurus

i

Pareiasuchus peringueyi Pareiasuchus ei Arganaceras Deltavjatia i e a i i i i

d baini Embrithosaurus ei

d Australothyris Nochelesaurus Bradysaurus seeleyi g d i e e de Lanthanosuchus Broomia 260 Provelosaurus i i i i de ei e ei i i i ei ag i Nyctiphruretus d Bashkyroleter mesensis

h Tokosaurus i chengi Belebey

e vegrandis Belebey Bashkyroleter bashkyricus Rhipaeosaurus i d maximi Belebey de d d e ad d c Acleistorhinus ei i d d d d 270 i ik c i MESOSAURIDAE d hi hi e Bolosaurus striatus i de ad 280 d i bc Permian Eudibamus Colobomycter pholeter Colobomycter Bolosaurus grandis Colobomycter vaughni Colobomycter Delorhynchus Feeserpeton Abyssomedon de ei i Microleter ac d c c c c a ei c c c d d i 290 ei

d c angustodunensis Belebey

i i Erpetonyx a i d 300 d c c i d ac c ei ad c 310 i ac cg c a ac i 320 c cg

c 330 c Carboniferous 340 cg cgh 350 b 230

240 Archosaurus Sarmatosuchus Elachistosuchus Boreopricea Moradisaurus Tasmaniosaurus Teyujagua Acerosodontosaurus MBCN 15730 Gansurhinus Aenigmastropheus 250 idd m h d a k k Thadeosaurus i g i k a e

k Saurorictus a i k de Eorasaurus i d k 260 e em

k Lanthanolania

d Rothianiscus c Labidosaurikos Captorhinikos chozaensis Captorhinikos gi aguti Captorhinikos valensis Captorhinikos 270 em c c bcf im c gi bc c c

i laticeps Captorhinus i ac Reiszorhinus i 280 Permian Triassic ac c i i c i c Protocaptorhinus Opisthodontosaurus Captorhinus magnus Captorhinus Orovenator i gi Thuringothyris b c c c c a Romeria prima 290 c c Romeria texana c c Rhiodenticulatus c c c

c Concordia Spinoaequalis c c c cg c c 300 c c

c Anthracodromeus bc Brouffia

Cephalerpeton c c a Coelostegus c a

c 310 c c c c c

c c c 320 c

c 330

Carboniferous ac c

340 c c ac 350

Fig. 6 Example of a reconstruction of ancestral geographic ranges of sauropsids. Tree was randomly selected from the 100 time calibrated trees. a Parareptilia. b Eureptilia. Node labels represent the geographic range of that node with the highest probability, deduced by BioGeoBEARS. a = Western Europe; b = Western North America; c = Eastern North America; d = Eastern Europe; e = East Asia; f = Northern South America; g = Northern Africa; h = Southern South America; i = Southern Africa; j = Antarctica; k = Madagascar; l = India; m = Australia

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a 230

240 Ictidorhinus

250 Burnetia

Paraburnetia i Lemurosaurus Herpetoskylax Lende Lycaenodon

i NHMUK R871 Niuksenitia Lobalopex Lophorhinus

i Proburnetia i d i i i i i i

i Hipposaurus Pachydectes Pampaphoneus Bullacephalus Jonkeria Heleosaurus Notosyodon Anteosaurus Elliotsmithia Styracocephalus d i i h BP 1 5678 Elliotsmithia 260 ei Syodon d c Ulemosaurus Australosyodon potens d Titanophoneus adamanteus i i c c i i d Ennatosaurus

i mirabilis i d d Archaeosyodon Pyozia ei Tapinocaninus Microsyodon Sinophoneus Varanodon Phreatophasma

i Angelosaurus romeri d Mesenosaurus c

d Raranimus Angelosaurus greeni hancocki Cotylorhynchus

d a Caseoides i Angelosaurus dolani Watongia Caseopsis e c bransoni Cotylorhynchus d d c d e halselli i c c a c a b a 270 i Casea nicholsi i d b pogonias Casea broilii Trichasaurus Dimetrodon limbatus Dimetrodon grandis Cotylorhynchus romeri Cotylorhynchus c i Secodontosaurus i Ruthenosaurus

i c c Glaucosaurus i c c c c c b c b

i Edaphosaurus cruciger i ei de c bc c d c d de c Permian Triassic

280 Dimetrodon borealis c b d i c c b

de Ctenorhachis Lupeosaurus Edaphosaurus boanerges Eothyris c Oromycter Ctenospondylus

c Euromycter

e Tambacarnifex ei c c i c Sphenacodon bc Edaphosaurus novomexicanus e e Dimetrodon milleri c c b

290 bc b Apsisaurus c c Ruthiromia ac Vaughnictis Oedaleops wellesi

de Pantelosaurus Aerosaurus greenleeorum Cutleria

Stereophallodon c a a c Callibrachion d c

Cryptovenator c

c b Datheosaurus c c bc i Archaeovenator e c Eocasea

a Edaphosaurus colohistion c c ch i d c Ianthodon Haptodus c Ianthasaurus 300 c c c e c c c c c hi c c c c c

e Archaeothyris c c c ch c c c ch c c c c c c 310 Echinerpeton bc ac c c c c b c c i bc c 320 ac c ac c ei c

330 ac c c Carboniferous

c 340 c

c ac c 350 c

b

250 Urumchia Tetracynodon darti Tetracynodon Progalesaurus Cynosaurus Eosimops Moschorhinus Cerdosuchoides Olivierosuchus Myosaurus Dinanomodon Regisaurus Kombuisia Pristerodon Robertia Promoschorhynchus Leontosaurus curvatus Lystrosaurus murrayi Lystrosaurus Lystrosaurus maccaigi Lystrosaurus declivis Lystrosaurus Moschowhaitsia Geikia elginensis Lystrosaurus hedini Lystrosaurus Kwazulusaurus Turfanodon Ictidosuchops Odontocyclops Interpresosaurus Daqingshanodon Delectosaurus Akidognathus Diictodon Vivaxosaurus

e ij ij i ij ij ij Dvinia i il i Gordonia i i il i ei i i i i i i i lacerticeps Dicynodontoides i e Jimusaria a d Aelurognathus Theriognathus Chthonosaurus

Daptocephalus i d i Rubidgea d e Annatherapsidus Elph e i Sycosaurus laticeps Nanictosaurus

d Basilodon Ictidosuchoides e i a Ictidochampsa d Peramodon il i i i d d i Gorgonops Tetracynodon tenuis Tetracynodon d i Pelanomodon Rhachiocephalus Scylacosuchus Mirotenthes

i i Smilesaurus Sintocephalus Kitchinganomodon Kawingasaurus Ruhuhucerberus Ictidostoma

Endothiodon i Dinogorgon Mupashi i Cistecephaloides Euchambersia Keyseria Sycosaurus nowaki Emydops oweni Emydops USNM PAL 412421 USNM PAL Syops Clelandina Ichibengops d Dicynodon huenei i TSK 2 Scylacosaurus SAM PK K8516 Galepus Digalodon Katumbia Arctognathus Emydops arctatus Emydops i Cistecephalus i

Tropidostoma ik Lycideops

Niassodon ai Hofmeyria i Geikia locusticeps i i i d i i i i i i il i Ictidosuchus i i i i i i i Charassognathus ij Aulacephalodon i i i i i i Sauroscaptor i i i i i i

i Abdalodon Suminia Australobarbarus i i Karenites i i i i i i Perplexisaurus i Euptychognathus l d i i i Bulbasaurus d d i SAM PK K10984 90 d i i i Viatkosuchus i i ai i Lycosuchus

ai i i d Glanosuchus i ai i

i Idelesaurus i i i ij i Pardosuchus Pristerognathus d i Prosictodon i i 260 i Galeops i d i i i

i i i Rastodon i i Alopecodon ai i i Choerosaurus i i Anomocephalus ad i i Brachyprosopus

i Galechirus il Tiarajudens ai i i h i i i i ij i i i i h ai i ai i ad i i ai ai i Eriphostoma Colobodectes i i Ulemica ai i i ai i i i i

i i Eodicynodon oelofseni d i i i Patranomodon i i Otsheria i i i Lanthanostegus

i Ictidosaurus

Eodicynodon oosthuizeni i i d i i i i i i i i i i hi i i i i i i i i d Biseridens i i e i i i i i 270 i i i i d i i

Permian Triassic i i i i i i i ai ai i i a i ij i

i i i

i i 280 i i i

i

Fig. 7 Example of a reconstruction of ancestral geographic ranges of Synapsids. Tree was randomly selected from the 100 time calibrated trees. a Pelycosaurian-grade synapsids, Biarmosuchia and Dinocephalia. b Neotherapsida. Node labels represent the geographic range of that node with the highest probability, deduced by BioGeoBEARS. a = Western Europe; b = Western North America; c = Eastern North America; d = Eastern Europe; e = East Asia; f = Northern South America; g = Northern Africa; h = Southern South America; i = Southern Africa; j = Antarctica; k = Madagascar; l = India; m = Australia

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a 220

230

240 Tupilakosaurus wetlugensis Tupilakosaurus Thabanchuia oomie Uranocentrodon senekalensis Uranocentrodon Broomistega putterelli stowi Saharastega Nigerpeton riclesi Laccosaurus watsoni primus 250 i BP 1 4473 i k di g g

i Rhineceps nyasaensis i Rhinesuchoides tenuiceps d Peltobatrachus putulatus Peltobatrachus Rhinesuchus capensis i Rhinesuchus broomianus i i i i Parapytanga catarinensis Parapytanga Serra do Cadeado Specimen Serra Konzhukovia sangabrielensis Konzhukovia Konzhukovia vetusta Konzhukovia

h h cosgriffiAustralerpeton Rhinesuchus whaitsi Melosaurus uralensis 260 h stuckenbergi Platyoposaurus

Tryphosuchus paucidens Tryphosuchus d Kamacops Zygosaurus h i d d d Collidosuchus d d tarda Konzhukovia Melosaurus kamaensis Platyoposaurus watsoni Platyoposaurus hi i d Melosaurus platyrhinus d

i Slaugenhopia texensis i d d d aspidephorus hi i d Eryops megacephalus di c Syndyodosuchus 270 Intasuchus silvicola insignis Trimerorhachis c i Clamorosaurus hottoni Gerobatrachus ik bc Dasyceps microphthalmus i Acheloma cumminsi Prionosuchus plummeri d d d Isodectes obtusus Aspidosaurus binasseri c multicinctus d Parioxys c hi nazariensis Procuhy c c anneae Timonya Broiliellus texensis f c c i di c c f c i f i 280 d di Permian Triassic Phonerpeton pricei Perryella olsoni Perryella Georgenthalia Rotaryus gothae Cacops woehri annectens Tambachia Acheloma dunni Pasawioops Cacops morrisi texensis Tersomius c Platyhistrix Chenoprosopus lewisi Scapanops neglecta Chenoprosopus milleri a Conjunctio a c Rubiostratilia c c c Broiliellus olsoni c a c serratus Zatrachys hauseri Branchierpeton amblystomum c Acroplous vorax Onchiodon labyrinthicus Acanthostomatops vorax

Apateon gracilis bc c c bc Sclerocephalus jogischeideri ac cb pedestris Reiszerpeton c Broiliellus brevis bc a a craigi Apateon flagrifer 290 a c Neldasaurus wrightae Leptorophus tener Actinodon frossardi Brevidorsum Leptorophus raschi a di Melanerpeton eisfeldi a Dasyceps bucklandi Glanochthon latirostris a Glanochthon angusta decheni Sclerocephalus nobilis Melanerpeton humbergense Palatinerpeton kraetschmeri Palatinerpeton

a Broiliellus reiszi Apateon kontheri Micromelerpeton credneri

Plemmyradytes c Sclerocephalus stambergi Ecolsonia cutlerensis Aconastes vesperus

Apateon caducus c Schoenfelderpeton prescheriSchoenfelderpeton a c d c a a a c a Sclerocephalus bavaricus a c

Apateon dracyiensis a a Cheliderpeton vranyi a Melanerpeton sembachense a a a a a c a ac b b d a Memonomenos dyscriton a

b POL F 2012 001 a cg c c c d a a Eoscopus lockardi c c a a a c d a Iberospondylus schultzei a c c c d Glaukerpeton

Actiobates a

a Fedexia 300 a c c c ad a ac ac c bc c ad c Isodectes punctulatus c Cochleosaurus bohemicus grandiceps Amphibamus ac Adamanterpeton ohioensis Platyrhinops lyelli Limnogyrinus elegans salamandoides c ac bc a a c Capetus palustris a c a c c cf a c a a c c a a a a Cochleosaurus florensis a a c Dendrepeton confusum 310 a a c ac acadianum bc c a c a c ac Procochleosaurus jarrowensis c a ad a ac bc c a a c a Eugyrinus wildi c c ac 320 c a a c c a c c c c ac a c a a c ac a c c c ac 330 c Balanerpeton woodi a ac a

a

340 Carboniferous c a a ac

a a 350 a a cg 360 a ac Devonian

b 230

240 Triassic 250 b Diplocaulus minimus g 260 sternbergi

270 Peronendon c Diplocaulus magnicornis Brachydectes Pariotichus Pelodosotis Hapsidopareion Quasicaecilia

Euryodus primus c Euryodus daylae c c c c c c c c bc c c 280 Permian Tambaroter Cardiocephalus peabodyi Nannaroter

c bonneri Proxilodon c c c a c

290 Stegotretus bc Saxonerpeton c Huskerpeton englehorni MNHN SOT II 101076 MNHN SOT Scincosaurus Altenganerpeton Diploceraspis c c b c a a Oestocephalus c a a Coloraderpeton ac c b Ophiderpeton 300 a scalarisSauropleura Phlegethontia linearis Sparodus Pseudophlegethontia Phlegethontia longissima Ptyonius

Diceratosaurus c ac c ac ac a ac c c a c c bc c a Batrachiderpeton c 310 c Asaphestera a c c c ac c galvani Keraterpeton c c a c c a a c c Acherontiscus ac Adelospondylus 320 c Utaherpeton b a a c c ac bc

330 c Dolichopareias Adelogyrinus a c a ac c Lethiscus

Carboniferous a a 340 ac a a ac a a 350 a a a a ac a a 360 a Devonian

Fig. 8 Example of a reconstruction of ancestral geographic ranges of amphibians. Tree was randomly selected from the 100 time calibrated trees. a Temnospondyli. b Lepospondyli. Node labels represent the geographic range of that node with the highest probability, deduced by BioGeoBEARS. a = Western Europe; b = Western North America; c = Eastern North America; d = Eastern Europe; e = East Asia; f = Northern South America; g = Northern Africa; h = Southern South America; i = Southern Africa; j = Antarctica; k = Madagascar; l = India; m = Australia

biogeographic history would evolve stochastically, with the same biogeographic the BioGeoBEARS analysis: the area-adjacency matrix limited the areas to which a events permitted as were allowed by the DIVA model. The probabilities of lineage could disperse, and the regions employed could not be further subdivided dispersal, vicariance and local occurring at any point in time along a i.e. a vicariance event could not occur at a node where the range covers only a lineage/at a node taken from the results of the BioGeoBEARS analysis. The possible single area. The R function to simulate the biogeographic history is provided in ranges of each node/lineage were constrained by the same parameters employed in Supplementary Data 5.

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Having simulated the 100 null histories and calculated the mean dispersal and biostratigraphy and Pangaean biogeography. Zool. J. Linn. Soc. 139, 157–212 vicariance rates of each, the null rates were subtracted from the observed rates. (2003). Thus, a negative dispersal/vicariance rate would indicate that the observed rate is 23. Modesto, S. P., Scott, D. M. & Reisz, R. R. A new parareptile with temporal less than would be expected given a randomly evolved biogeographic history over fenestration from the Middle Permian of . Can. J. Earth Sci. 46, the same phylogeny. 9–20 (2009). 24. Liu, J., Rubidge, B. S. & Li, J. New basal supports Laurasian origin for . Acta Palaeontol. Pol. 54, 393–400 (2009). Code availability . All custom code used in this study is available in Supplementary 25. Tsuji, L. A., Müller, J. & Reisz, R. R. Microleter mckinzieorum gen. et sp. nov. Data 5. from the Lower Permian of : the basalmost parareptile from Laurasia. J. Syst. Palaeontol. 8, 245–255 (2010). Data availability 26. Cleal, C. J. et al. Late Moscovian terrestrial biotas and palaeoenvironments All data generated and analysed during this study are included in this published of Variscan Euramerica. Neth. J. Geosci. 88, 181–278 (2009). article (and its supplementary information files). A reporting summary for this 27. Kessler, J. L. L., Soreghan, G. S. & Wacker, H. Equatorial aridity in western article is available as a Supplementary Information file. Pangaea: Lower Permian loessite and dolomitic palaeosols in northeastern . J. Sediment. Res. 71, 817–832 (2001). 28. Rees, P. M. et al. Permian phytogeographic patterns and climate data/model Received: 30 April 2018 Accepted: 8 November 2018 comparisons. J. Geol. 110,1–31 (2002). 29. Tabor, N. J. & Poulsen, C. J. Palaeoclimate across the Late Pennsylvanian–Early Permian tropical palaeolatitudes: a review of climate indicators, their distribution and relation to palaeophysiographic climate factors. Palaeogeogr. Palaeoclim. 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