Deleterious alleles in the context of domestication, inbreeding, and selection

Abstract

Each individual has a certain number of harmful mutations in its genome. These mutations can lower the fitness of the individual carrying them, dependent on their dominance and selection coefficient. Effective population size, selection, and admixture are known to affect the occurrence of such mutations in a population. The relative roles of demography and selection are a key in understanding the process of adaptation. These are factors that are potentially influenced and confounded in domestic animals. Here, we hypothesize that the series of events of bottlenecks, introgression, and strong artificial selection associated with domestication increased mutational load in domestic species. Yet, mutational load is hard to quantify, so there are very few studies available revealing the relevance of evolutionary processes. The precise role of artificial selection, bottlenecks, and introgression in further increasing the load of deleterious variants in animals in breeding and conservation programmes remains unclear. In this paper, we review the effects of domestication and selection on mutational load in domestic species. Moreover, we test some hypotheses on higher mutational load due to domestication and selective sweeps using sequence data from commercial pig and chicken lines. Overall, we argue that domestication by itself is not a prerequisite for genetic erosion, indicating that fitness potential does not need to decline. Rather, mutational load in domestic species can be influenced by many factors, but consistent or strong trends are not yet clear. However, methods emerging from molecular genetics allow discrimination of hypotheses about the determinants of mutational load, such as effective population size, inbreeding, and selection, in domestic systems. These findings make us rethink the effect of our current breeding schemes on fitness of populations.

Assessing genomic diversity and signatures of selection in Original Braunvieh cattle using whole-genome sequencing data

“…In agreement with previous studies in cattle [21], missense deleterious and high impact variants occurred predominantly at low allele frequency likely indicating that variants which disrupt physiological protein functions are removed from the population through purifying selection [65]. However, deleterious variants may reach high frequency in livestock populations due to, e.g., the frequent use of individual carrier animals in artificial insemination [66], hitchhiking with favorable alleles under artificial selection [67,68], or demography effects such as population bottlenecks [69]. Because we predicted functional consequences of missense variants using computational inference, they have to be treated with caution in the absence of experimental validation [70].…”

Unlocking the origins and biology of domestic animals using ancient DNA and paleogenomics

“…Another feature of domestication that has been explored using population genomics and paleogenomics of livestock and companion animal populations is the documented increase in deleterious genetic variation that has been termed the "cost of domestication" [182,183]. The intellectual roots of this concept can again be traced back to Charles Darwin and also to Alfred Russel Wallace, both of whom suggested that the benign "conditions of life" for domestic animals may ultimately have negative consequences in terms of evolutionary fitness [154,184].…”

The genomics of domestication special issue editorial

“…This issue has five broad topics, with the first focused on deleterious mutations in the context of domestication (Bosse, Megens, Derks, de Cara, & Groenen, ; Plekhanova, Nuzhdin, Utkin, & Samsonova, ). Bosse et al.…”

“…Bosse et al. () use data from pig and chickens to explore mutational load, finding that domestication does not necessitate a reduction in fitness, but rather specific species‐level factors impact the extent to which deleterious mutations accumulate in domestic populations. They make the important point that whether a mutation is deleterious or not may be context dependent.…”

“…This issue has five broad topics, with the first focused on deleterious mutations in the context of domestication (Bosse, Megens, Derks, de Cara, & Groenen, 2018;Plekhanova, Nuzhdin, Utkin, & Samsonova, 2018). Bosse et al (2018) use data from pig and chickens to explore mutational load, finding that domestication does not necessitate a reduction in fitness, but rather specific species-level factors impact the extent to which deleterious mutations accumulate in domestic populations. They make the important point that whether a mutation is deleterious or not may be context dependent.…”