Abstract
BackgroundSpecies domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species. These include not only inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, but also post-divergence gene flow and introgression. Although domestication potentially affects the occurrence of both desired and undesired mutations, the way wild relatives of domesticated species evolve and how expensive the genetic cost underlying domestication is remain poorly understood. Here, we investigated the demographic history and genetic load of chicken domestication.ResultsWe analyzed a dataset comprising over 800 whole genomes from both indigenous chickens and wild jungle fowls. We show that despite having a higher genetic diversity than their wild counterparts (average π, 0.00326 vs. 0.00316), the red jungle fowls, the present-day domestic chickens experienced a dramatic population size decline during their early domestication. Our analyses suggest that the concomitant bottleneck induced 2.95% more deleterious mutations across chicken genomes compared with red jungle fowls, supporting the “cost of domestication” hypothesis. Particularly, we find that 62.4% of deleterious SNPs in domestic chickens are maintained in heterozygous states and masked as recessive alleles, challenging the power of modern breeding programs to effectively eliminate these genetic loads. Finally, we suggest that positive selection decreases the incidence but increases the frequency of deleterious SNPs in domestic chicken genomes.ConclusionThis study reveals a new landscape of demographic history and genomic changes associated with chicken domestication and provides insight into the evolutionary genomic profiles of domesticated animals managed under modern human selection.
Highlights
Species domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species
Our analyses suggest that the concomitant bottleneck induced 2.95% more deleterious mutations across chicken genomes compared with red jungle fowls, supporting the “cost of domestication” hypothesis
In the first phase of our 1K Chicken Genomes Project (1K Chicken Genome Project (CGP); https://bigd.big.ac.cn/chickensd/), through sequencing and analyzing 863 genomes from both jungle fowls and indigenous chickens sampled across South, Southeast, and East Asia as well as Europe, we demonstrated that all domestic chickens were monophyletic, derived from an red jungle fowl (RJF) lineage of G. g. spadiceus (GGS) whose present-day range is predominantly in northern Thailand, southwestern China, and Myanmar, and regained genetic diversity via introgression from additional RJF subspecies and jungle fowl species during their dispersals out of the domestication center [27]
Summary
Species domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species These include inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, and postdivergence gene flow and introgression. All organisms carry a certain level of deleterious mutations in their genomes, which can potentially affect their fitness [1, 2] The majority of these harmful mutations are detrimental and recessive—only a few are dominant or recessive lethal [3]. The “cost of domestication” hypothesis was proposed to explain this general pattern observed in these domestic species [17] It suggests that bottlenecks along with domestication reduced the power of purifying selection to remove deleterious variants, resulting in a dramatic accumulation of deleterious variants in domesticated species. Genomic assessment of pigs [20], bees [21], and some crops [18] exhibited no significant historical decline in their genetic diversity relative to respective wild progenitors
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