Selective constraints in cold-region wild boars may defuse the effects of small effective population size on molecular evolution of mitogenomes

Abstract

Spatial range expansion during population colonization is characterized by demographic events that may have significant effects on the efficiency of natural selection. Population genetics suggests that genetic drift brought by small effectivepopulation size (Ne) may undermine the efficiency of selection, leading to a fasteraccumulation of nonsynonymous mutations. However, it is still unknown whetherthis effect might be balanced or even reversed by strong selective constraints. Here,we used wild boars and local domestic pigs from tropical (Vietnam) and subarcticregion (Siberia) as animal model to evaluate the effects of functional constraints andgenetic drift on shaping molecular evolution. The likelihood-ratio test revealed thatSiberian clade evolved significantly different from Vietnamese clades. Differentdatasets consistently showed that Siberian wild boars had lower Ka/Ks ratios thanVietnamese samples. The potential role of positive selection for branches with higherKa/Ks was evaluated using branch-site model comparison. No signal of positive selection was found for the higher Ka/Ks in Vietnamese clades, suggesting the interclade difference was mainly due to the reduction in Ka/Ks for Siberian samples. Thisconclusion was further confirmed by the result from a larger sample size, amongwhich wild boars from northern Asia (subarctic and nearby region) had lower Ka/Ksthan those from southern Asia (temperate and tropical region). The lower Ka/Ksmight be due to either stronger functional constraints, which prevent nonsynonymous mutations from accumulating in subarctic wild boars, or larger Ne in Siberianwild boars, which can boost the efficacy of purifying selection to remove functionalmutations. The latter possibility was further ruled out by the Bayesian skyline plotanalysis, which revealed that historical Ne of Siberian wild boars was smaller than thatof Vietnamese wild boars. Altogether, these results suggest stronger functionalconstraints acting on mitogenomes of subarctic wild boars, which may provide newinsights into their local adaptation of cold resistance.