Contrasting mode of evolution at a coat color locus in wild and domestic pigs

Abstract

Despite having only begun approximately 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.

Figure 1. Amino acid sequence conservation within wild boar is sharply contrasted by the sequence diversity amongst MC1R alleles found within domestic pigs.

(A) The observed number of synonymous and non-synonymous substitutions amongst Chinese and European domestic pigs and amongst Chinese and European wild boars; included amongst the “non-synonymous” substitutions is the two base pair insertion associated with the E^P allele. The diversity of coat color among domestic pigs is exemplified by the images on the left and contrasted with the camouflaged coat color in the wild boar on the lower right. (B) A Median-joining network of MC1R alleles in Asian and European pigs. All known alleles are represented by circles while squares represent predicted intermediate forms that have not yet been found. Thin black lines placed perpendicular to the lines connecting the individual haplotypes represent single, synonymous changes, and thicker red lines represent non-synonymous changes. The asterisk placed near the two black lines leading to alleles *0104 and *0203 indicates the only instance of an identical mutation at different locations on the tree. Colors inside the circles and squares depict the observed and predicted coat colors associated with a given allele; question marks inside two of the squares indicate that the associated coat color of these intermediate alleles cannot be predicted because they connect alleles that differ by two non-synonymous substitutions. The first two digits in the nomenclature for porcine MC1R alleles alongside the circles indicate the associated coat color phenotype: 01 = wild type, 02 = dominant black, Asian form, 03 = dominant black, European form, 04 = recessive red, and 05 = black spotting. The two last digits are used to distinguish alleles that are associated with the same phenotype. (C) Wild boar sow with piglets in the nest. Note the remarkable camouflage coat color pattern in the piglets. (Photo: Anneli Andersson, Linköping University, Sweden.)