Large-scale genomic analysis reveals the genetic cost of chicken domestication

Abstract

Background Species 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. Results We 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. Conclusion This 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.

Detection of selection signatures in South African Mutton Merino sheep using whole‐genome sequencing data

“…SAMM had a highest linkage disequilibrium level, followed by Chinese Merino and Australian Merino (Figure S1). These results were consistent with the observations in other domestic animals including dogs (Gou et al, 2015), pigs (Muñoz et al, 2019), chickens (Wang et al, 2021;Xu et al, 2021), and ducks (Guo et al, 2021), indicating that domestication and artificial selection induced a loss of genetic diversity and an increase of inbreeding.…”

Domestication obscures genomic estimates of population history

“…Studies also showed that linked selection and population structure could bias Sequentially Markovian Coalescent model inferences (Johri et al, 2021; Mazet et al, 2016). In addition, psmc might misestimate splitting times between domestical species and their wild relatives because this model does not take into account the possible effect of admixture (Wang et al, 2021). However, few studies have examined whether recent fluctuations in population size (<1,000 years ago) may influence psmc inferences.…”

“…Many studies have applied psmc to investigate the population history of extinct or endangered species (Hu et al, 2020; Hung et al, 2014; Saremi et al, 2019), date the divergence time between sister species (Westbuty et al, 2019), and examine interactions between historical climate fluctuations and population changes (Mays et al, 2018; Nadachowska‐Brzyska et al, 2015). psmc has also been used to infer the demographic history of domesticated species and estimate when the domesticated species (or their progenitors) split from their wild relatives (Wang et al, 2021). Despite the popularity and reliability of psmc for tracing demographic history back to hundreds of thousands of years ago, few studies have explored how recent population changes (e.g., recent population bottlenecks) may affect psmc inferences.…”

Large-Scale Whole Genome Sequencing Study Reveals Genetic Architecture and Key Variants for Breast Muscle Weight in Native Chickens

“…Furthermore, a parallel allele frequency pattern, based on synonymous and missense variants, was obtained that was consistent with observed patterns in humans and cattle [ 47 , 48 ]. Wang et al defined high-impact SNPs as having a PROVEAN score < −2.5 for missense variants [ 12 ]. Herein, we focused on frequency changes between the two chicken lines and conservation status, to evaluate chicken phenotype high-impact variants rather than on PROVEAN score for missense SNPs.…”

“…Therefore, comparison of the original line and the selected line is an excellent means by which to dissect genetic architecture and explore the genes affecting BrW. Wang et al revealed a new landscape of genomic changes associated with domestication by investigating the high-impact (missense) single nucleotide polymorphisms (SNPs), which were determined by low PROVEAN score [ 12 ]. Thus, it is conducive to identify the genes that respond to artificial selection by studying the missense SNPs in JX chicken.…”