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Untangling the Evolutionary History of European Bison (Bison Bonasus) Ayla L

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Untangling the Evolutionary History of European Bison (Bison Bonasus) Ayla L bioRxiv preprint doi: https://doi.org/10.1101/467951; this version posted November 11, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Untangling the Evolutionary History of European Bison (Bison bonasus) Ayla L. van Loenen1, Emilia Hofman-Kaminska´ 2, Kieren J. Mitchell1, Bastien Llamas1, Herve´ Bocherens3, Julien Soubrier1,4, Holly Heiniger1, Martina Pacher5, Daniel Makowiecki6, Giedre˙ Piliciauskien˘ e˙ 7, Dorothee´ Drucker8, Rafał Kowalczyk2, and Alan Cooper1 1Australian Centre for Ancient DNA (ACAD), University of Adelaide, Australia 2Mammal Research Institute Polish Academy of Sciences, Stoczek 1, 17-230, Białowie˙za,Poland 3Fachbereich Geowissenschaften, Forschungsbereich Palaobiologie,¨ Universitat¨ T ¨ubingen, Holderlinstr.¨ 12, D-72074 T ¨ubingen, Germany 4Genetics and Molecular Pathology, SA Pathology, Adelaide, South Australia 5000, Australia 5Institut f ¨urPalaontologie,¨ Universitat¨ Wien, Geozentrum, UZA II, Althanstraße 14, A - 1090 Wien, Austria 6Faculty of History, Institute of Archeology Nicolaus Copernicus University, ul. Gagarina 11, 87-100 Torun,´ Poland details 7Faculty of History, Vilnius University, Universitetofor str. 7, Vilnius 01122, Lithuania 8Universitat¨ T ¨ubingen Senckenberg Center for Human Evolution and Palaeoenvironment (HEP), Holderlinstr.¨ DOI 12, D-72074 T ¨ubingen, Germany Corresponding author: Ayla L. van Loenenmanuscript1 WITHDRAWNEmail address:see [email protected] ABSTRACT European bison (Bison bonasus) are the largest endemic vertebrates in Europe, and one of the few megafaunal species to have survived the mass megafaunal extinction during the Pleistocene/Holocene transition (12-9 thousand years ago). Untangling their evolutionary history would provide valuable information about the response of European megafauna to periods of rapid environmental change. However, a severe and recent population bottleneck obscures much of the population history that could be inferred from the genomes of modern individuals. While several studies have attempted to analyse ancient European bison populations directly using ancient DNA, their datasets were limited in temporal and geographic range. In this study we present the most comprehensive dataset of ancient European bison mitochondrial genomes to date, with 131 ancient bison samples from across the Eurasian continent covering over 50 thousand years. We reveal patterns of bison distribution and concurrent environmental changes across a broad geographical and temporal range. In particular, population expansions following periods of extensive forest reduction combined with a decrease in anthropogenic pressures suggest that European bison remain preferentially adapted to an open steppe environment through to the present day. INTRODUCTION European bison (also known as wisent or Bison bonasus) are one of the few megafaunal species to have survived the Late Pleistocene/early Holocene megafaunal extinctions in Europe (Bocherens et al., 2015; Cooper et al., 2015). While formerly distributed across the continent during the Late Pleistocene and Holocene alongside the now extinct steppe bison (Bison priscus), European bison were restricted to two populations representing two subspecies by the end of the 19th century: one in the Białowieza˙ forest in Eastern Europe (Bison bonasus bonasus) and the other in the Caucasus Mountains (Bison bonasus caucasus) (Pucek, 2004; Krasinska´ and Krasinski,´ 2013; W˛eceket al., 2016). By the 1920s, both populations were extinct in the wild, with only a handful of individuals - comprising the recent bioRxiv preprint doi: https://doi.org/10.1101/467951; this version posted November 11, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. descendants of only 12 individuals - remaining in captivity (Pucek, 2004; Benecke, 2005; Krasinska´ and Krasinski,´ 2013). As a result of this severe bottleneck, modern European bison have significantly reduced genetic diversity (Wójcik et al., 2009; Tokarska et al., 2009, 2011; Massilani et al., 2016; Soubrier et al., 2016; W˛eceket al., 2016). Such dramatic bottleneck events typically obscure long-term patterns of evolutionary history (Chang and Shapiro, 2016), and the evolution and palaeobiogeography of European bison consequently remain poorly understood. Several recent studies have investigated the evolutionary history of European bison using ancient DNA (aDNA) (Soubrier et al., 2016; Massilani et al., 2016; Onar et al., 2017; Marsolier-Kergoat et al., 2015; Grange et al., 2018). The data presented in these studies comprised predominantly mitochondrial D-loop data plus a handful of mitochondrial genomes (where most specimens were from either the Urals Mountains or France). These geographically and temporally limited data supported the division of ancient European bison into two distinct mitochondrial clades (wisent and CladeX in Soubrier et al. (2016); or Bb2 and Bb1 in Massilani et al. (2016) and Grange et al. (2018)). Hereafter, we will refer to these clades according to the Bb1/Bb2 nomenclature from Massilani et al. (2016) and Grange et al. (2018), where ’Bb1’ refers to the extinct Late Pleistocene population with a distinct mitochondrial clade and ’Bb2’ refers to the living European bison (and also ancient specimens that are more closely related to living European bison than they are to Bb1). It has additionally been suggested that Bb2, Bb1 and steppe bison potentially reflect distinct taxa adapted to specific ecological niches in the two regions covered by these studies (Urals mountains, Russia, and France) (Soubrier et al., 2016; Massilani et al., 2016). However, this hypothesis has not been tested at a continental scale, and the exact geographical and temporal distribution of individuals belonging to the two mitochondrial clades remainsdetails to be characterised. In this paper, we present 81 new ancient mitochondrialfor genome sequences from bison specimens from across Eurasia spanning over 50 thousand years, substantially increasing both the spatial and temporal coverage of the previously available data. ByDOI adding these new data to previously published sequences we assembled a total dataset comprising 131 bison mitochondrial genomes. In addition, each new specimen is radiocarbon dated and associated with dietary isotopic information. Using the increased resolution provided by this dataset,manuscript we compared our refined reconstruction of the evolutionary history of European WITHDRAWNbison tosee concurrent environmental and climatic changes. RESULTS Sequencing results Seventy-nine mitochondrial genomes were successfully sequenced with more than 70% coverage and an average depth ≥3. Two additional partial mitochondrial genomes were sequenced with coverage between 40-70% and average depth greater than 0.4, which was sufficient to identify the taxonomic affiliation of both specimens (A17406 and A17482). Damage patterns were consistent with ancient DNA (Supplementary Table 1), with additional details of sequencing and mapping summary statistics output from PALEOMIX given in Supplementary Table 2. Specimens were assigned to clades of European bison for subsequent analyses according to their position in an initial ML tree (Supplementary Figure 1). Out of the 131 Eurasian bison included in this study, 102 specimens were directly dated and ranged in age from greater than 50,000 calBP (calibrated radiocarbon years before present) to modern day (Supplementary Table 3). The remaining 29 specimens were undated, but 22 came from well-characterised archaeological layers that provided an associated date range for the specimens. Phylogenetic analysis The median-joining haplotype network (Figure 2) clearly shows three distinct groups within the mito- chondrial genome diversity: two clades of European bison (referred to as Bb1 and Bb2 as per Massilani et al. (2016) and Grange et al. (2018)), and steppe bison. There was no obvious genetic structure within the European bison clades (i.e. no obvious geographic clusters, and no distinctions between B. b. bonasus and B. b. caucasus). All three groups (steppe bison, Bb1 and Bb2) were present in Europe until the Pleistocene/Holocene transition (∼9-12 kya), at which point there was a clear reduction in bison diversity in Europe with only Bb2 surviving until the present (Figure 2, Supplementary File 1). The GMRF (Gaussian Markov Random Field) Bayesian skyride plot of Bb1 specimens did not show any evidence of population change over time prior to their extinction, while the GMRF Bayesian skyride plot of Bb2 specimens suggested a population decline starting ∼10 kya (Figure 3). The two distinct European bison clades are significantly less differentiated from each other than either is from the steppe bison (81 base 2/15 bioRxiv preprint doi: https://doi.org/10.1101/467951; this version posted November 11, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. changes between Bb1 and Bb2, compared to 286 base changes between steppe bison and Bb2). However, the available mitochondrial
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