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Keywords:

  • agouti;
  • genetic drift;
  • natural selection;
  • overdominance;
  • pigmentation

A fundamental goal for evolutionary biologists is to connect the processes of natural selection and genetic drift with the maintenance of genetic variation in the wild. There are now scores of examples in which mapping phenotypes to genotypes has identified the molecular basis of traits in natural populations, but documenting the fitness consequences of these genes has proven more elusive. A long-term study of several thousand unmanaged sheep on the remote Scottish island of Hirta in the St. Kilda archipelago provides a unique opportunity to make these connections between genotype, phenotype and fitness. Since 1985, there has been a steady decline in the frequency of sheep with a rare uniform (‘self’-) pigmentation pattern as opposed to the more common wild-type pattern of dark upper body and pale belly. In this issue of Molecular Ecology, Gratten et al. (2012) link variation at the agouti signalling protein (ASIP) gene with 25 years of pedigree information and individual fitness data to investigate the contributions of natural selection and genetic drift to this decline. Consistent with the decrease in frequency of self-type sheep, Gratten et al. demonstrate that recessive genetic variants at ASIP are associated with reduced lifetime fitness. But surprisingly, these variants show the opposite trend to the self-type phenotype by increasing throughout the study period. This paradoxical result occurs because heterozygotes that harbour the majority of self-type alleles have increased in frequency. This pattern would not have been detectable if only phenotype had been monitored because the pigmentation pattern of heterozygotes is indistinguishable from that of wild-type homozygotes. The study provides an excellent example of the importance of measuring selection at both the phenotypic and genetic level, and demonstrates how long-term pedigrees can be used to link alleles to phenotypes and ultimately to fitness.