Genomic basis of circannual rhythm in the european corn borer moth

Abstract

ABSTRACTGenetic variation in life-history timing allows populations to synchronize with seasonal cycles but little is known about the molecular mechanisms that produce differences in circannual rhythm in nature. Changes in diapause timing in the European corn borer moth (Ostrinia nubilalis) have facilitated rapid response to shifts in winter length encountered during range expansion and from climate change, with some populations emerging from diapause earlier to produce an additional generation per year. We identify genomic variation associated with changes in the time spent in winter diapause and show evidence that the circadian clock genes period (per) and pigment dispersing factor receptor (Pdfr) interact to underlie this adaptive polymorphism in circannual rhythm. Per and Pdfr are located within two epistatic QTL, strongly differ in allele frequency among individuals that pupate earlier or later, have the highest linkage disequilibrium among gene pairs in the QTL regions despite separation by > 4 megabases, and possess amino-acid changes likely to affect function. One per mutation in linkage disequilibrium with Pdfr creates a novel putative clock-cycle binding site found exclusively in populations that pupate later. We find associated changes in free-running daily circadian rhythm, with longer daily rhythms in individuals that end diapause early. These results support a modular connection between circadian and circannual timers and provide testable hypotheses about the physiological role of the circadian clock in seasonal synchrony. Winter length is expected to continually shorten from climate warming and we predict these gene candidates will be targets of selection for future adaptation and population persistence.