Contrasting Mode of Evolution at a Coat Color Locus in Wild and Domestic Pigs

Abstract

Despite having only begun ∼10,000 years ago, the process of domestication has resulted in a degree of phenotypic variation within individual species normally associated with much deeper evolutionary time scales. Though many variable traits found in domestic animals are the result of relatively recent human-mediated selection, uncertainty remains as to whether the modern ubiquity of long-standing variable traits such as coat color results from selection or drift, and whether the underlying alleles were present in the wild ancestor or appeared after domestication began. Here, through an investigation of sequence diversity at the porcine melanocortin receptor 1 (MC1R) locus, we provide evidence that wild and domestic pig (Sus scrofa) haplotypes from China and Europe are the result of strikingly different selection pressures, and that coat color variation is the result of intentional selection for alleles that appeared after the advent of domestication. Asian and European wild boar (evolutionarily distinct subspecies) differed only by synonymous substitutions, demonstrating that camouflage coat color is maintained by purifying selection. In domestic pigs, however, each of nine unique mutations altered the amino acid sequence thus generating coat color diversity. Most domestic MC1R alleles differed by more than one mutation from the wild-type, implying a long history of strong positive selection for coat color variants, during which time humans have cherry-picked rare mutations that would be quickly eliminated in wild contexts. This pattern demonstrates that coat color phenotypes result from direct human selection and not via a simple relaxation of natural selective pressures. This study addresses why coat colors of domestic animals are so variable, while those of their wild ancestors are so uniform. Specifically, we asked whether this was the result of (i) relaxed purifying selection, (ii) that some mutations affect both coat color and another trait under strong selection (for instance behavior), or (iii) direct human selection for altered coat color phenotypes. We investigated genetic variation in the melanocortin receptor 1 (MC1R) gene among wild and domestic pigs from both Europe and Asia. Though we found a similar number of mutations in wild and domestic pigs, the nature of the mutations was strikingly different. All mutations found among wild boars were silent, i.e., they did not change the protein sequence. This implies strong purifying selection in the wild that maintains camouflage coat color. In contrast, nine out of ten mutations found in domestic pigs altered the protein sequence, thereby drastically transforming the resulting coat color. These results demonstrate that early farmers intentionally selected pigs with novel coat coloring. Their motivations could have been as simple as a preference for the exotic or selection for reduced camouflage to facilitate animal husbandry and/or to make the domesticated forms distinct from their wild ancestor.