The duration of dormancy regulates seasonal timing in many organisms and may be modulated by day length and temperature. Though photoperiodic modulation has been well studied, temperature modulation of dormancy has received less attention. Here, we leverage genetic variation in diapause in the apple maggot fly, Rhagoletis pomonella, to test whether gene expression during winter or following spring warming regulates diapause duration. We used RNAseq to compare transcript abundance during and after simulated winter between an apple-infesting population and a hawthorn-infesting population where the apple population ends pupal diapause earlier than the hawthorn-infesting population. Marked differences in transcription between the two populations during winter suggests that the ‘early’ apple population is developmentally advanced compared with the ‘late’ hawthorn population prior to spring warming, with transcripts participating in growth and developmental processes relatively up-regulated in apple pupae during the winter cold period. Thus, regulatory differences during winter ultimately drive phenological differences that manifest themselves in the following summer. Expression and polymorphism analysis identify candidate genes in the Wnt and insulin signaling pathways that contribute to population differences in seasonality. Both populations remained in diapause and displayed a pattern of up- and then down-regulation (or vice versa) of growth-related transcripts following warming, consistent with transcriptional repression. The ability to repress growth stimulated by permissive temperatures is likely critical to avoid mismatched phenology and excessive metabolic demand. Compared with diapause studies in other insects, our results suggest some overlap in candidate genes/pathways, though the timing and direction of changes in transcription are likely species specific.
The authors declare no competing or financial interests.
P.J.M., G.J.R., T.H.Q.P., D.A.H. and J.L.F. conceived the gene expression study, P.J.M. and G.J.R. designed the gene expression experiments, S.H.B., H.M.R. and G.J.R. conceived the 454 SNP study, P.J.M. performed the gene expression experiments, S.H.B., H.M.R. and K.K.O.W. performed the 454 SNP study, P.J.M., G.J.R., S.H.B., H.M.R. and K.K.O.W. analyzed the data, and all authors contributed to manuscript drafting.
This work was supported by funds from the University of Notre Dame Environmental Change initiative, US Department of Agriculture, and National Science Foundation IOS 1451274 to G.J.R. and J.L.F., National Science Foundation IOS 1257298, the Florida Agricultural Experiment Station, and the joint Food and Agriculture Organization/International Atomic Energy Agency (FAO/IAEA) CRP Dormancy Management to Enable Mass-rearing to D.A.H., and US Department of Agriculture AG 2007-35604-17886 to H.M.R. and S.H.B.
All raw sequence reads have been deposited in the NCBI Short Read Archive, accessible through BioProject Accession PRJNA324814. The transcriptome assembly is deposited in the NCBI Transcriptome Shotgun Assembly archive under accession GETQ00000000.1. Supplementary tables and scripts are deposited in Dryad: http://dx.doi.org/10.5061/dryad.51db2.
- Received March 24, 2016.
- Accepted June 14, 2016.
- © 2016. Published by The Company of Biologists Ltd