Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila
Alan O. Bergland, Emily L. Behrman, Katherine R. O’Brien, Paul S. Schmidt, Dmitri A. Petrov
(Submitted on 20 Mar 2013)
In many species, genomic data have revealed pervasive adaptive evolution indicated by the near fixation of beneficial alleles. However, when selection pressures are highly variable along a species range or through time adaptive alleles may persist at intermediate frequencies for long periods. So called balanced polymorphisms have long been understood to be an important component of standing genetic variation yet direct evidence of the ubiquity of balancing selection has remained elusive. We hypothesized that environmental fluctuations between seasons in a North American orchard would impose temporally variable selection on Drosophila melanogaster and consequently maintain allelic variation at polymorphisms adaptively evolving in response climatic variation. We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection. We show that adaptively oscillating polymorphisms are often millions of years old, predating the divergence between D. melanogaster and D. simulans and that a subset of these polymorphisms respond predictably to an acute frost event. Taken together, our results demonstrate that rapid temporal fluctuations in climate over generational scales is a predominant force that maintains adaptive alleles and promotes genetic diversity.