  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.
