Establishing the validity of domestication genes using DNA from ancient chickens

Significance Recent studies have identified the genetic basis of numerous traits that differentiate modern domestic species from their wild counterparts. In both plants and animals, traits (and the genes underlying them) found ubiquitously in modern breeds are often presumed to have been selected early during the domestication process. Here, by determining genetic variability in ancient European chickens over the past 2,000 years, we show that a mutation thought to be crucial during chicken domestication was not subjected to strong human-mediated selection until much later in time. This result demonstrates that the ubiquity of mutations, which differentiate modern wild and domestic taxa, does not necessarily imply ancient origins. Modern domestic plants and animals are subject to human-driven selection for desired phenotypic traits and behavior. Large-scale genetic studies of modern domestic populations and their wild relatives have revealed not only the genetic mechanisms underlying specific phenotypic traits, but also allowed for the identification of candidate domestication genes. Our understanding of the importance of these genes during the initial stages of the domestication process traditionally rests on the assumption that robust inferences about the past can be made on the basis of modern genetic datasets. A growing body of evidence from ancient DNA studies, however, has revealed that ancient and even historic populations often bear little resemblance to their modern counterparts. Here, we test the temporal context of selection on specific genetic loci known to differentiate modern domestic chickens from their extant wild ancestors. We extracted DNA from 80 ancient chickens excavated from 12 European archaeological sites, dated from ∼280 B.C. to the 18th century A.D. We targeted three unlinked genetic loci: the mitochondrial control region, a gene associated with yellow skin color (β-carotene dioxygenase 2), and a putative domestication gene thought to be linked to photoperiod and reproduction (thyroid-stimulating hormone receptor, TSHR). Our results reveal significant variability in both nuclear genes, suggesting that the commonality of yellow skin in Western breeds and the near fixation of TSHR in all modern chickens took place only in the past 500 y. In addition, mitochondrial variation has increased as a result of recent admixture with exotic breeds. We conclude by emphasizing the perils of inferring the past from modern genetic data alone.