Species-specific responses of Late Quaternary megafauna to climate and humans

Despite decades of research, the roles of climate and humans in driving the dramatic extinctions of large-bodied mammals during the Late Quaternary remain contentious. We use ancient DNA, species distribution models and the human fossil record to elucidate how climate and humans shaped the demographic history of woolly rhinoceros, woolly mammoth, wild horse, reindeer, bison and musk ox. We show that climate has been a major driver of population change over the past 50,000 years. However, each species responds differently to the effects of climatic shifts, habitat redistribution and human encroachment. Although climate change alone can explain the extinction of some species, such as Eurasian musk ox and woolly rhinoceros, a combination of climatic and anthropogenic effects appears to be responsible for the extinction of others, including Eurasian steppe bison and wild horse. We find no genetic signature or any distinctive range dynamics distinguishing extinct from surviving species, underscoring the challenges associated with predicting future responses of extant mammals to climate and human-mediated habitat change. Toward the end of the Late Quaternary, beginning c. 50,000 years ago, Eurasia and North America lost c. 36% and 72% of their large-bodied mammalian genera (megafauna), respectively1. The debate surrounding the potential causes of these extinctions has focused primarily on the relative roles of climate and humans2,3,4,5. In general, the proportion of species that went extinct was greatest on continents that experienced the most dramatic Correspondence and requests for materials should be addressed to E.W (ewillerslev@snm.ku.dk). *Joint first authors †Deceased Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Author contributions E.W. initially conceived and headed the overall project. C.R. headed the species distribution modelling and range measurements. E.D.L. and J.T.S. extracted, amplified and sequenced the reindeer DNA sequences. J.B. extracted, amplified and sequenced the woolly rhinoceros DNA sequences; M.H. generated part of the woolly rhinoceros data. J.W., K-P.K., J.L. and R.K.W. generated the horse DNA sequences; A.C. generated part of the horse data. L.O., E.D.L. and B.S. analysed the genetic data, with input from R.N., K.M., M.A.S. and S.Y.W.H. Palaeoclimate simulations were provided by P.B., A.M.H, J.S.S. and P.J.V. The directly-dated spatial LAT/LON megafauna locality information was collected by E.D.L., K.A.M., D.N.-B., D.B. and A.U.; K.A.M. and D.N-B performed the species distribution modelling and range measurements. M.B. carried out the gene-climate correlation. A.U. and D.B. assembled the human Upper Palaeolithic sites from Eurasia. T.G. and K.E.G. assembled the archaeofaunal assemblages from Siberia. A.U. analysed the spatial overlap of humans and megafauna and the archaeofaunal assemblages. E.D.L., L.O., B.S., K.A.M., D.N.-B., M.K.B., A.U., T.G. and K.E.G. wrote the Supplementary Information. D.F., G.Z., T.W.S., K.A-S., G.B., J.A.B., D.L.J., P.K., T.K., X.L., L.D.M., H.G.M., D.M., M.M., E.S., M.S., R.S.S., T.S., E.S., A.T., R.W., A.C. provided the megafauna samples used for ancient DNA analysis. E.D.L. made the figures. E.D.L, L.O. and E.W. wrote the majority of the manuscript, with critical input from B.S., M.H., K.A.M., M.T.P.G., C.R., R.K.W, A.U. and the remaining authors. Mitochondrial DNA sequences have been deposited in GenBank under accession numbers JN570760-JN571033. Reprints and permissions information is available at www.nature.com/reprints. NIH Public Access Author Manuscript Nature. Author manuscript; available in PMC 2014 June 25. Published in final edited form as: Nature. ; 479(7373): 359–364. doi:10.1038/nature10574. N IH -P A A uhor M anscript N IH -P A A uhor M anscript N IH -P A A uhor M anscript climatic changes6, implying a major role of climate in species loss. However, the continental pattern of megafaunal extinctions in North America approximately coincides with the first appearance of humans, suggesting a potential anthropogenic contribution to species extinctions3,5. Demographic trajectories of different taxa vary widely and depend on the geographic scale and methodological approaches used3,5,7. For example, genetic diversity in bison8,9, musk ox10 and European cave bear11 declines gradually from c. 50–30,000 calendar years ago (ka BP). In contrast, sudden losses of genetic diversity are observed in woolly mammoth12,13 and cave lion14 long before their extinction, followed by genetic stability until the extinction events. It remains unresolved whether the Late Quaternary extinctions were a cross-taxa response to widespread climatic or anthropogenic stressors, or were a species-specific response to one or both factors15,16. Additionally, it is unclear whether distinctive genetic signatures or geographic range-size dynamics characterise extinct or surviving species— questions of particular importance to the conservation of extant species. To disentangle the processes underlying population dynamics and extinction, we investigate the demographic histories of six megafauna herbivores of the Late Quaternary: woolly rhinoceros (Coelodonta antiquitatis), woolly mammoth (Mammuthus primigenius), horse (wild Equus ferus and living domestic Equus caballus), reindeer/caribou (Rangifer tarandus), bison (Bison priscus/Bison bison) and musk ox (Ovibos moschatus). These taxa were characteristic of Late Quaternary Eurasia and/or North America and represent both extinct and extant species. Our analyses are based on 846 radiocarbon-dated mitochondrial DNA (mtDNA) control region sequences, 1,439 directly-dated megafaunal remains, and 6,291 radiocarbon determinations associated with Upper Palaeolithic human occupations in Eurasia. We reconstruct the demographic histories of the megafauna herbivores from ancient DNA data, model past species distributions and determine the geographic overlap between humans and megafauna over the last 50,000 years. We use these data to investigate how climate change and anthropogenic impacts affected species dynamics at continental and global scales, and contributed to in the extinction of some species and the survival of others. Effects of climate change differ across species and continents The direct link between climate change, population size and species extinctions is difficult to document10. However, population size is likely controlled by the amount of available habitat and is indicated by the geographic range of a species17,18. We assessed the role of climate using species distribution models, dated megafauna fossil remains and palaeoclimatic data on temperature and precipitation. We estimated species range sizes at the time periods of 42, 30, 21 and 6 ka BP as a proxy for habitat availability (Fig. 1; Supplementary Information section S1). Range size dynamics were then compared to demographic histories inferred from ancient DNA using three distinct analyses (Supplementary Information section S3): (i) coalescent-based estimation of changes in effective population size through time (Bayesian skyride19), which allows detection of changes in global genetic diversity; (ii) serial coalescent simulation followed by Approximate Bayesian Computation, which selects among different models describing continental population dynamics; and (iii) isolation-by-distance analysis, which estimates Lorenzen et al. Page 2 Nature. Author manuscript; available in PMC 2014 June 25. N IH -P A A uhor M anscript N IH -P A A uhor M anscript N IH -P A A uhor M anscript potential population structure and connectivity within continents. If climate was a major factor driving species population sizes, we would expect expansion and contraction of a species’ geographic range to mirror population increase and decline, respectively. We find a positive correlation between changes in the size of available habitat and genetic diversity for the four species—horse, reindeer, bison and musk ox—for which we have range estimates spanning all four time-points (the correlation is not statistically significant for reindeer: p = 0.101) (Fig. 2; Supplementary Information section S4). Hence, species distribution modelling based on fossil distributions and climate data are congruent with estimates of effective population size based on ancient DNA data, even in species with very different life-history traits. We conclude that climate has been a major driving force in megafauna population changes over the past 50,000 years. It is noteworthy that both estimated modelled ranges and genetic data are derived from a subset of the entire fossil record (Supplementary Information sections S1 and S3). Thus, changes in effective population size and range size may change with the addition of more data, especially from outside the geographical regions covered by the present study. However, we expect that the reported positive correlation will prevail when congruent data are compared. The best-supported models of changes in effective population size in North America and Eurasia during periods of dramatic climatic change during the past 50,000 years are those in which populations increase in size (Fig. 3, Supplementary Information section S3). This is true for all taxa except bison. However, the timing is not synchronous across populations. Specifically, we find highest support for population increase beginning c. 34 ka BP in Eurasian horse, reindeer and musk ox (Fig. 3a). Eurasian mammoth and North American horse increase prior to the Last Glacial Maximum (LGM) c. 26 ka BP. Models of population increase in woolly rhinoceros and North American mammoth fit equally well before and after the LGM, and North American reindeer populations increase later still. Only North American bison shows a population decline (Fig. 3b), the intensity of which likely swamps the signal of global population increase starting at c. 35 ka BP identified in the skyride plot