Incomplete lineage sorting rather than hybridization explains the inconsistent phylogeny of the wisent

Kun Wang,Tao Ma,Jianquan Liu,Quanjun Hu,Johannes A Lenstra,Liang Liu,Qiang Qiu

doi:10.1038/s42003-018-0176-6

Abstract

The wisent or European bison is the largest European herbivore and is completely cross-fertile with its American relative. However, mtDNA genome of wisent is similar to that of cattle, which suggests that wisent emerged as a hybrid of bison and an extinct cattle-like species. Here, we analyzed nuclear whole-genome sequences of the bovine species, and found only a minor and recent gene flow between wisent and cattle. Furthermore, we identified an appreciable heterogeneity of the nuclear gene tree topologies of the bovine species. The relative frequencies of various topologies, including the mtDNA topology, were consistent with frequencies of incomplete lineage sorting (ILS) as estimated by tree coalescence analysis. This indicates that ILS has occurred and may well account for the anomalous wisent mtDNA phylogeny as the outcome of a rare event. We propose that ILS is a possible explanation of phylogenomic anomalies among closely related species.

Highlights

The wisent or European bison is the largest European herbivore and is completely crossfertile with its American relative
The wisent and American bison are morphologically similar and cross-fertile and have closely related nuclear genes[17,18], but the Mitochondrial DNA (mtDNA) phylogeny consistently clusters the wisent with the lineage leading to taurine cattle and zebu[19]
This was confirmed by analysis of separate autosomes (Supplementary Figure 2), species tree estimated by MP-EST(Maximum Pseudo-likelihood for Estimating Species Trees)[25] and Astral[26] (Supplementary Figure 3) and by orthologous gene trees

Summary

Results

The Bovini phylogeny and the anomalous position of the wisent mtDNA genome. Genetic distances within a sliding window of 500 kb yielded very similar profiles for the bison–cattle and wisent–cattle comparisons (Pearson's correlation coefficient = 0.91) (Fig. 1a). Diverged species (taurine and zebu cattle; bison and wisent) exhibit relatively large numbers of identical-by-descent segments. On the basis of the f4 ratio test, the proportion of cattle ancestry was estimated to be 2.7%, 2.0%, 4.0%, 1.2%, and 1.0% in yak, bison, Caucasus, wisent founder, and Modern[2] populations, respectively (Supplementary Table 6). In a part of chromosome 1, bison is closer to taurine cattle (Fig. 2e), which is not observed on other chromosomes (Supplementary Figure 7) This suggests relatively recent gene flow between bison and taurine cattle, which is consistent with shared identity by descent. These results reveal a complex population history of the wisent with variable levels of cattle ancestry. It should be noted that the percentages of mtDNA topology in gene trees may underestimate the level of gene flow in the past, since during subsequent generations the introgressed regions would have been fragmented by recombination events

Conclusions

Methods

E European bison