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.
