Traces of hybridization among closely related species have been found everywhere it was looked for, including the genus Homo. Bovines are no exception to this. About ten years ago, it was proposed that the wisent, which I refer to as Bos bison bonasus here, originated as a hybrid of aurochs and steppe bison, Bos bison priscus, and inherited around 10% of its nuclear genome from aurochs. Now, ten years later, it has been demonstrated that this hypothesis was based on premature conclusions and partly also the result of methodological problems. However, the rebuttal of the hybrid origin hypothesis did not nearly attract as much attention as the paper by Soubrier et al., 2016, so that many still think this is the current state of research. Considering that I wrote a post when the paper came out titled “Confirmed: the wisent is an aurochs hybrid” back then in 2016 that is still online, I feel obliged to present a (hopefully) up-to-date picture of the current research on the origin of the European bison. Let’s dive into the literature.
A possible hybrid origin for the wisent was first proposed in 2004 by Verkaar et al., when it was surprisingly revealed that the wisent does not cluster with American bison and yak on the mitochondrial genome but with taurine and indicine cattle instead [1]. This would have suggested that bison bulls repeatedly mated with cows of the cattle lineage, which, given the time and region, would have been aurochs, giving rise to a bison that has “cattle-line mitochondria”. Then, more than ten years later, this hypothesis was endorsed by Soubrier et al., who executed a test of 10.000 single nucleotide polymorphisms and concluded that 10,9% of the nuclear genome of the wisent stem from aurochs [2]. At that time, I found that convincing, given that wisent sometimes clearly show the primigenius spiral in their horns and have a shorter body length than American bison, traits that I associated with the aurochs. But, as we will see, the results of Soubrier et al., did not remain uncontested for long.
The first critical response to mention would be Wang et al from two years later [3]. They find no evidence of 10% nuclear aurochs ancestry, and also found that parts of the nuclear genome show a similar phylogeny as the mitochondrial genome. The authors consider it more likely that the evolutionary phenomenon called incomplete lineage sorting is responsible for the weird mitogenomic position of the wisent on the phylogenetic tree.
ILS is a rather cool phenomenon. It happens when there are polymorphic genes (with more than one allele) in an ancestral population and the population splits up and undergoes cladogenesis. One branch would inherit only one allele of the polymorphic gene (let’s call it “A”), while the other population still has the alleles A and B. Then, this other population splits up too and one filial population retains only A, and the other one only B. What would the result on a phylogenic tree be if you look at this gene? The population that branched off first would group together with the population that retained A, while B would result as the outgroup to the other two – although this is not what happened in reality. This is incomplete lineage sorting. In fact, it is not rare that mitogenomes show phylogenies that are inconsistent with those inferred from nuclear DNA [3]. Wang et al. find that ILS is a more plausible explanation for the mitochondrial position of the wisent and more consistent with the genomic structure of the bovine [3]. The authors also caution that phylogenies based on single genes can be misleading because of ILS [3].
What about the 10% aurochs ancestry on the mitochondrial genome? It seems that this number is erroneous because an inadequate method was used [4]. Soubrier et al. looked at fewer than 10.000 SNP, which is a rather scarce sample, and did an f4-statistics analysis with them, which is how they arrived at the 10,9% aurochs ancestry. Grange et al. point out that this might be problematic because f4-statistics assume an ancestral population that is polymorphic for the SNPs, while the sample the authors used were from the BovineSNP50 chip that contains SNPs for differentiating individuals of modern cattle breeds [4]. With another approach, namely the Approximate Bayesian Computation (ABC), Grange et al. arrive at a 97,2% probability that there is at least one percent aurochs ancestry in the wisent genome, which is significantly lower than the results of Soubrier et al. [4]. The method employed by Soubrier et al. also results in ancient wisents, wisents from 1911 and Pleistocene priscus being closer to each other than the wisent from 1911 to modern wisents, indicating that something is methodologically wrong here [4].
Weçek et al. did a whole genome sequence analysis with modern wisent genomes as well as four historical samples and found that only 2,4 to 3,2% of the wisent genome seem to come from the aurochs/cattle lineage and the genomic structure suggests that it occurred a long time ago, therefore they consider it possible that this reflects aurochs introgression but they note it requires more research [5].
If the wisent is not an aurochs hybrid, where does it come from? One hypothesis that was postulated is that it is a descendant of late surviving B. b. schoetensacki. Bone remains from the Sirejol cave from the Upper Pleistocene have been tentatively morphologically assigned to this form previously, and a phylogenetic analysis revealed that the material belonged to the Clade X proposed by Soubrier et al. and Bb1 proposed by Massilani et al. (2016) [6]. The authors of Palacio et al. therefore conclude that schoetensacki corresponds with this mitochondrial clade [6]. The presence of schoetensacki in the Late Pleistocene would imply a ghost lineage spanning over a 500.000-year period, since this variant disappears from the fossil record shortly after aurochs enter the European continent in the Middle Pleistocene.
However, the morphological assignment of the Sirejol material to schoetensacki was likely premature, as a morphometric analysis taking sexual dimorphism into account rejects that this material was of a late surviving schoetensacki bison [4]. The much more basal B. b. schoetensacki clusters morphologically with the earlier B. b. menneri, but not with steppe bison and wisent.
So the wisent is not a descendant of the European Bos bison schoetensacki either. What we can say is that molecular clock data suggests that the lineages of B. b. bonasus and B. b. bison diverged around 215kya (roughly the same time when B. b. priscus first entered America) and gene flow ceased at 102kya [4]. 57 ancient genomes suggest that late Pleistocene steppe bison originated from the north while wisent originate from a refuge in the southern Caucasus after the most recent glacial maximum [7]. The American bison is nested in the priscus tree on the mitogenome [4], so we can be rather confident that B. b. bison descends from B. p. priscus in some way (either directly or over B. b. latifrons).
The two mitochondrial clades Bb1 and Bb2 are present in the late Pleistocene in Western Europe and the Caucasus, they are sister clades to the modern wisent clade [7,8]. It seems that while aurochs retreated southwards during glacial periods, ancient bison stayed in refuges dispersed over Europe [7,8]. This fragmentation and isolation could explain how the ancestors of the wisent split off from the rest of late Pleistocene bison around 215kya. While the more cold-adapted ancestors of the steppe bison/American bison clade probably remained in the north, the ancestors of the wisent might have stayed in their refuges in the Caucasus and parts of Europe.
As you see, the situation is much more nuanced than my post from 2016 suggests. It is a reminder for me that the last word is never spoken in science, contrary to what the title of my 2016 post suggests (“confirmed”, a word I should not have used).
If I missed any relevant papers in this post, I'd be grateful if it could be pointed out to me.
Literature
[1] Verkaar et al.: Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? 2004.
[2] Soubrier et al.: Early cave art and ancient DNA record the origin of European bison. 2016.
[3] Wang et al.: Incomplete lineage sorting rather than hybridization explains the inconsistent phylogeny of the wisent. 2018.
[4] Grange et al.: The evolution and population diversity of bison in Pleistocene and Holocene Eurasia: sex matters. 2018.
[5] Weçek et al.: Complex admixture preceded and followed the extinction of wisent in the wild. 2016.
[6] Palacio et al.: Genome data on the extinct Bison schoetensacki establish it as a sister species of the extant European bison (Bison bonasus). 2017.
[7] Massilani et al.: Past climate changes, population dynamics and the origin of Bison in Europe. 2016.
[8] wisenthybrid3
[9] Zver et al.: Phylogeny of Late Plesitocene and Holocene Bison species in Europe and North America. 2021.
