The Evolution and Population Diversity of Bison in Pleistocene and Holocene Eurasia: Sex Matters

Abstract

Knowledge about the origin and evolutionary history of the bison has been improved recently owing to several genomic and paleogenomic studies published in the last two years, which elucidated large parts of the evolution of bison populations during the Upper Pleistocene and Holocene in Eurasia. The produced data, however, were interpreted in contradicting manners. Here, we have gathered, reanalyzed and compared previously published or unpublished morphometric and genetic data that have not yet been integrated and that we synthesize in a unified framework. In particular, we re-estimate dates of divergence of mitogenome lineages based on an extended dataset comprising 81 complete ancient bison mitogenomes and we revisit putative gene flow between the Bos and Bison genera based on comparative analyses of ancient and modern bison genomes, thereby questioning published conclusions. Morphometric analyses taking into account sexual dimorphism invalidate a previous claim that Bison schoetensacki was present in France during the Late Pleistocene. Both morphometric and genome analyses reveal that Eurasian bison belonging to different Bison priscus and Bison bonasus lineages maintained parallel evolutionary paths with gene flow during a long period of incomplete speciation that ceased only upon the migration of B. priscus to the American continent establishing the American bison lineage. Our nuclear genome analysis of the evolutionary history of B. bonasus allows us to reject the previous hypothesis that it is a hybrid of B. priscus and Bos primigenius. Based on present-day behavioral studies of European and American bison, we propose that apparently conflicting lines of evidence can be reconciled by positing that female bison drove the specialization of bison populations to different ecological niches while male bison drove regular homogenizing genetic exchanges between populations.

Untangling the Evolutionary History of European Bison (Bison bonasus)

“…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).…”

“…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).…”

“…The median-joining haplotype network (Figure 2) clearly shows three distinct groups within the mitochondrial 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.…”

“…all available specimens from Eurasia identified as either Bb1, Bb2, B. bonasus or B. priscus) available on NCBI and ENA. Two genome sequences were not included, one was chimeric (KY055664, Węcek et al (2016)), and the other being sourced from a hyena coprolite (GAO1/KU886087, Palacio et al (2017)) and with a contentious taxonomic origin (Grange et al, 2018). The resulting final dataset included 131 bison mitochondrial genomes from Eurasia.…”

“…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).…”