Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila

Abstract

In many species, genomic data have revealed pervasive adaptive evolution indicated by the 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 strength of balancing selection and the stability and prevalence of balanced polymorphisms 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 to 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 these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes. In addition, we show that adaptively oscillating polymorphisms are likely millions of years old, with some likely predating the divergence between D. melanogaster and D. simulans. Taken together, our results demonstrate that rapid temporal fluctuations in climate over generational time promotes adaptive genetic diversity at loci affecting polygenic phenotypes.