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 effective population size (N e) may undermine the efficiency of selection, leading to a faster accumulation of nonsynonymous mutations. However, it is still unknown whether this effect might be balanced or even reversed by strong selective constraints. Here, we used wild boars and local domestic pigs from tropical (Vietnam) and subarctic region (Siberia) as animal model to evaluate the effects of functional constraints and genetic drift on shaping molecular evolution. The likelihood‐ratio test revealed that Siberian clade evolved significantly different from Vietnamese clades. Different datasets consistently showed that Siberian wild boars had lower Ka/Ks ratios than Vietnamese samples. The potential role of positive selection for branches with higher Ka/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. This conclusion was further confirmed by the result from a larger sample size, among which wild boars from northern Asia (subarctic and nearby region) had lower Ka/Ks than those from southern Asia (temperate and tropical region). The lower Ka/Ks might be due to either stronger functional constraints, which prevent nonsynonymous mutations from accumulating in subarctic wild boars, or larger N e in Siberian wild boars, which can boost the efficacy of purifying selection to remove functional mutations. The latter possibility was further ruled out by the Bayesian skyline plot analysis, which revealed that historical N e of Siberian wild boars was smaller than that of Vietnamese wild boars. Altogether, these results suggest stronger functional constraints acting on mitogenomes of subarctic wild boars, which may provide new insights into their local adaptation of cold resistance.
Highlights
Evaluating the relative contributions of selection and genetic drift in shaping genome evolution is one of the central issues in population and evolutionary biology
As we found that Siberian wild boars had lower Ka/Ks than Vietnamese wild boars, it is very interesting to evaluate whether this reduced Ka/Ks ratio in Siberian wild boars might come from higher Ne in Siberian wild boars
Both the pairwise Ka/ Ks and the best model determined by model selection with associated LRT show that Siberian wild boars have a significantly lower Ka/Ks than Vietnamese wild boars and free-range local pigs, suggesting stronger selective constraints in mitogenomes of Siberian wild boars
Summary
Evaluating the relative contributions of selection and genetic drift in shaping genome evolution is one of the central issues in population and evolutionary biology. In terms of gene functions, mitochondria are well identified as the power station of cells for thermogenesis and thermoregulation upon which the basic physiological processes are possible (Block, 1994; Rowland, Bal, & Periasamy, 2015; Skulachev, 1999) Owing to these strong functional constraints in mitochondria, the evolution of mtDNA is maintained mainly by purifying selection to remove the accumulation of deleterious nonsynonymous mutations (Sun, Shen, Irwin, & Zhang, 2011). Considering the effect of “Out-of-Southeast Asia” dispersal or limited gene flow due to geographic isolation, Ne(s) of wild boars in cold regions are expected to be smaller This rationale may lead to an opposite inference that purifying selection in cold regions might be less effective to remove deleterious mutations than that in tropical areas due to genetic drift. The major objectives of this study include the following: (a) based on phylogenetic structure of both Vietnamese and Siberian wild boars (and local pigs) to evaluate the potential differences in tempos of accumulation of slightly deleterious mutation; and (b) to evaluate the causes of these differences in the context of selective constraints and Ne
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