Genomic basis of circannual rhythm in the European corn borer moth

Authors: KOZAK, GENEVIEVE - University Of Massachusetts; WADSWORTH, CHRSITA - Tufts University; KAHNE, SHOSHANNA - Tufts University; BOGDANOWICZ, STEVEN - Cornell University; HARRISON, RICHARD - Cornell University; Coates, Brad; DOPMAN, ERIK - Tufts University

Submitted to: Current Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/20/2019
Publication Date: 10/10/2019
Citation: Kozak, G.M., Wadsworth, C.M., Kahne, S.C., Bogdanowicz, S.M., Harrison, R.G., Coates, B.S., Dopman, E.B. 2019. Genomic basis of circannual rhythm in the European corn borer moth. Current Biology. 29(20):3501-3509. https://doi.org/10.1016/j.cub.2019.08.053.
DOI: https://doi.org/10.1016/j.cub.2019.08.053

Interpretive Summary: Non-migratory arthropods persist in a given local environmental through the selection for responses to temperature and day-length that maximize survival and reproduction with respect to seasonal changes. Locally adapted insects pests of corn, including larvae of the European corn borer (ECB), can cause significant levels of plant damage which reduce yields and profits among producers. Populations of ECB show differences is duration of a dormant larval overwintering state, called diapause, and the number of adult reproducing generations per year which are both influenced by local environmental queues to collectively determine a voltinism trait. Specifically, univoltine populations have a genetically-fixed single generation per year and are confined to the northern Corn Belt, whereas multivoltine populations are genetically-capable of greater than one generation based on the local environmental and are more widely distributed. Univoltine and multivoltine ECB can co-occur in the same locality, and show mating period asynchrony that may reduce gene flow and impact the spread of alleles that confer insecticide resistance. Furthermore, producers in regions where univoltine and multivoltine ECB co-occur are under greater economic pressure due to increased threats of ECB feeding damage. The genes that cause differences in voltinism are yet to be determined. An ARS researcher in collaboration with university scientists used a combined whole genome sequencing, population genomics, and genetic fine mapping approach to show that changes in two genes, period and pigment dispersing factor receptor, interact to control voltinism in ECB. This is the first research reporting the genes that determine voltinism in ECB, and may be applicable to all species of Lepidoptera. These data will be of interest to regulators, and university, government, and industry scientists interested in the adaptation of insect pests to changes local environmental conditions and shifts in the corresponding levels of crop damage.

Technical Abstract: Genetic 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. Changes in diapause timing in the European corn borer moth (Ostrinia nubilalis) have allowed rapid response to shifts in winter length encountered during range expansion and from human-induced climate change, with some regionally-adapted 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 is within encodes 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 predicted to continually shorten from climate warming and we predict these gene candidates will be targets of selection for future adaptation and population persistence.