Accumulation of slightly deleterious mutations in the mitochondrial genome: A hallmark of animal domestication

Abstract

The hypothesis that domestication lead to a relaxation of purifying selection on mitochondrial (mt) genomes was tested by comparative analysis of mt genes from dog, pig, chicken, and silkworm. The three vertebrate species showed mt genome phylogenies in which domestic and wild isolates were intermingled, whereas the domestic silkworm (Bombyx mori) formed a distinct cluster nested within its closest wild relative (B. mandarina). In spite of these differences in phylogenetic pattern, significantly greater proportions of nonsynonymous SNPs than of synonymous SNPs were unique to the domestic populations of all four species. Likewise, in all four species, significantly greater proportions of RNA-encoding SNPs than of synonymous SNPs were unique to the domestic populations. Thus, domestic populations were characterized by an excess of unique polymorphisms in two categories generally subject to purifying selection: nonsynonymous sites and RNA-encoding sites. Many of these unique polymorphisms thus seem likely to be slightly deleterious; the latter hypothesis was supported by the generally lower gene diversities of polymorphisms unique to domestic populations in comparison to those of polymorphisms shared by domestic and wild populations.

Population size may shape the accumulation of functional mutations following domestication

“…Previous studies have observed faster accumulation of non-silent mutations following domestication in some animals, including dog, pig, yak and chicken, which is believed to be a consequence of a decrease in N e associated with domestication and relaxation of purifying selection on mitochondrial genes in some domesticated species [ 2 , 16 , 17 ], but the debate on whether all domesticated animals exhibit a consistent trend is still ongoing [ 40 ]. Considering large N e differences across species, it would be very interesting to investigate whether the accumulation of functional mutations post- and pre-domestication might exhibit interspecific heterogeneities.…”

“…Quantitatively, the magnitude of selection is commonly measured by the ratio of the number of nonsynonymous substitutions per nonsynonymous site (Ka) to the number of synonymous substitutions per synonymous site (Ks) - Ka/Ks (or ω ); where ω < 1 indicates purifying selection, ω = 1 - neutral selection, and ω > 1 - positive selection [ 12 – 14 ]. Variations in selection strength may tune the amount of mutations: studies have found that domesticated animals accumulate functional mutations in some mitochondrial genes much faster than their wild relatives, in part due to the relaxed purifying selection [ 2 , 15 – 17 ]. However, apparently, relaxation of purifying selection is only one of the possible directions of changes in selection strength, especially for nuclear genomes.…”

Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species

“…For example, higher ratios of non-synonymous to synonymous changes in mitogenomes of a number of domesticated (cf. wild) taxa have been attributed to both relaxed selective constraint on metabolic efficiency because of human actions (for example, provision of resources and improved living conditions) and reduced efficiency of selection owing to repeated population bottlenecks during the domestication process (Hughes, 2013). In our case, rigorously distinguishing among metabolic adaptation to coastal environments (positive selection), small effective population in coastal environments (reduced efficiency of selection) and reduced metabolic constraint in coastal environments (relaxed selection) would be impossible without controlled experiments and/or studies of protein biochemistry.…”

Domestication Genomics: Evidence from Animals

“…The relaxation of selective constraint since domestication is hypothesized to be reflected in the coding regions of the mitochondrial genome that encodes energy metabolism genes (126). An excess of (slightly) deleterious mutations, that is, nonsynonymous mutations and mutations in RNA-encoding genes, has been characterized in the mitochondrial genomes of domesticated animals, such as the dog (126)(127)(128), pig (127), yak (129), and chicken (127). The low-coverage genomic-sequence data also revealed that a higher frequency of nonsynonymous mutations occurred in dogs compared with wolves (130).…”