Adaptation driven by novel mutations or from selection on standing genetic variation?

Our collegue Hopi Hoekstra at Harvard University in the US, who visited us in August last year, has a paper in one of the last issues of Science. You can read a brief report on the website Science Daily here.

At first I was not very excited about this paper, as it appears to be the usual story about the melanocortin receptor (MC1R) and how it affects coat colour patterns in various mice populations, a story that by know is sufficiently wellknown and established so one wonders what remains to be discovered.

MC1R is responsible for dark coat colour in mice that occur in dark habitats (see above), e. g. on the dark lava flows in Arizona, that Hopi Hoekstra has previously studied together with her colleague Michael Nachmann.

However, this new paper has a new twist: it appears as if selection has acted on a novel mutant in deer mice in Nebraska, and this novel that apparently appeared in the population shortly after the last Ice Age, about 8 000 years ago.

Catherine Linnen and Hopi have analyzed genetic variation among these different mice populations and estimated the age of the allele that causes light coat colour in the mice. Light coloured mice carry a certain allele at a gene called Agouti, and this allele is quite young as it shows evidence of a selective sweep through reduction in DNA sequence diversity around that particular allele. Linnen and Hoekstra have thus used the well-known statistical approach of coalescense analysis to infer the age of the novel mutation at the Agouti locus that is causing light coat colour.

This result is important, as it provides some contrast to recent suggestions that novel mutations might not be that important in cases of rapid evolutionary change, which have instead emphasize selection on standing genetic variation in rapid evolutionary change. For instance, rapid evolutionary change need not always to rely on standing genetic variation as suggested by the findings from other systems like sticklebacks. The alternative is instead that rapid adaptive change is driven by a process by which selection in novel environments "picks up" and favours alleles that already segregated in the ancestral population, rather than "waiting" for the emergence of rare novel beneficial mutations (that might take long time to appear).

This process is sometimes also called phenotype sorting, referring to how a polymorphic and variable base populations might become transformed in to a new (monomorphic and less variable) population through the selective increase and selective loss of already existing phenotypes, which are then "filtered" by selection in the novel environment. Something along these lines appears to also be the case in the freshwater isopods that we have studied in our group, and we discussed this earlier this year in a paper published in Journal of Evolutionary Biology, which you can find here.

In summary, the relative importance of selection acting on novel mutations vs. standing genetic variation is probably something that will be discussed a lot the coming years in evolutionary biology and ecology.