Domesticated genes gone wild

Artificial selection of domesticated plants and animals has been cited as a test case for natural selection since Charles Darwin first conceived the latter concept. But we generally consider that these two forms of selection operate to very different ends—that the features that make crops and livestock most useful to humans are unrelated to, or even contrary to, features that make them best suited to life in the wild. Many domesticated figs produce seedless fruit, which would be a selective dead end without farmers to propagate the trees by cuttings; and domesticated foxes are probably not cautious enough to survive long away from human care.
However, in at least one case study, the opposite seems to be true. Results from a study recently published in Molecular Ecology suggest that two gene variants that are doing quite well in a population of wild sheep on the Scottish islands of Saint Kilda probably originated in domesticated flocks.
The wild Soay sheep of Saint Kilda have coats of different colors. Those differences in coat color have a known genetic basis, and the underlying gene variants are associated with differences in fitness—all the raw ingredients necessary for natural selection to operate. Two loci are involved in the coat color variation. Sheep with one or two copies of a particular variant at the TYRP1 locus have dark wool, and sheep carrying two copies of an alternate variant have light wool; and sheep with one or two copies of the “light” TYRP1 variant have higher fitness than sheep with two copies of the “dark” variant—and long-term studies have show the light variant is becoming more common [PDF].
Variants at a different locus, ASIP, determine whether or not the wool on a sheep’s belly is the same color as the wool on its back (“self color”) or lighter (“wild”). The variant of ASIP associated with the wild coat pattern is dominant, so sheep with one or two copies have light-colored bellies; sheep with two copies of the self variant have the uniform self-coat coloring. Self-coated sheep are also less likely to survive to adulthood than wild-coated sheep—but self-coated sheep have greater reproductive success if they survive. These conflicting selective forces seem to have increased the frequency of sheep carrying one copy of the self-coat variant even as the frequency of self-coated sheep declines.
This previous work already provides some remarkably fine-grained understanding of the genetic basis of traits related to fitness. But it may be possible to add another detail: the origin of the selected coat-color variants. The Soay sheep haven’t been completely isolated from other breeds. In recent centuries, they shared the Saint Kilda islands with humans, who kept domesticated sheep—providing several hundred years of opportunity for what geneticists call “an admixture event,” and everyone else calls “sex,” between the Soay breed and those domesticated sheep. Humans and domestic livestock were evacuated from the islands in 1930, and the wild Soay sheep have had no known contact with other sheep since.
So the new study, lead-authored by Philine Feulner, digs into the population genetics of the Soay sheep and an international sample of domestic and wild sheep to pinpoint the origin of these selected coat-color variants.
Using data from high-throughput genotyping methods—a genotyping chip with about 50 thousand markers, developed for use with domestic sheep—the authors first tested to see whether Soay sheep had been, um, admixing with domestic sheep from Boreray sheep, a breed kept on the Saint Kilda islands. Using the STRUCTURE algorithm, they found that every individual in their sample of Soay sheep shared genetic ancestry with the Boreray sample. By simulating genetic data, they also demonstrated that this pattern was very unlikely to arise simply because all three sheep populations share a common ancestor sometime before humans started keeping sheep.
Then the authors zeroed in on variation in the vicinity of the TYRP1 and ASIP loci. When new genetic variants are introduced into a population by, um, admixture, they usually come with a long stretch of genetic code. Over time, recombination will break up this new code and mutation will add new variation on top of it—but in the relatively short term, the recipient population and the donor population share a long stretch of genetic sequence. So the authors compared the genetic sequence near TYRP1 and ASIP in Soay sheep to the sequence in the same region of samples from dozens of other sheep breeds. In both cases, the Soay sample had substantially longer stretches of sequence in common with samples from Borerary sheep than any other breed.
So it looks as though the coat-color variation in wild Soay sheep has a decidedly non-wild origin. The gene variants introduced into the Soay population have persisted over the decades since humans and their sheep left the Saint Kilda archipelago thanks to their fitness effects. In a sense, that’s like discovering a population of wolves with the flat faces of bulldogs.
References
Feulner PGD, J Gratten, JW Kijas, PM Visscher, JM Pemberton, and J Slate. 2013. Introgression and the fate of domesticated genes in a wild mammal population. Molecular Ecology 22:4210-21. doi: 10.1111/mec.12378.
Gratten J, AJ Wilson, AF McRae, D Beraldi, PM Visscher, JM Pemberton, and J Slate. 2008. A localized negative genetic correlation constrains microevolution of coat color in wild sheep. Science 319:318-20. doi: 10.1126/science.1151182.
Gratten J, JG Pilkington, EA Brown, TH Clutton-Brock, JM Pemberton, and J Slate. 2012. Selection and microevolution of coat pattern are cryptic in a wild population of sheep. Molecular Ecology 21:2977-90. doi: 10.1111/j.1365-294X.2012.05536.x.