Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

Abstract

Rapid evolutionary change in seasonal timing can facilitate ecological speciation and resilience to climate warming. However, the molecular mechanisms behind shifts in animal seasonality are still unclear. Evolved differences in seasonality occur in the European corn borer moth (Ostrinia nubilalis), in which early summer emergence in E-strain adults and later summer emergence in Z-strain adults is explained by a shift in the length of the termination phase of larval diapause. Here, we sample from the developmental time course of diapause in both strains and use transcriptome sequencing to profile regulatory and amino acid changes associated with timing divergence. Within a previously defined quantitative trait locus (QTL), we nominate 48 candidate genes, including several in the insulin signaling and circadian rhythm pathways. Genome-wide transcriptional activity is negligible during the extended Z-strain termination, whereas shorter E-strain termination is characterized by a rapid burst of regulatory changes involved in resumption of the cell cycle, hormone production and stress response. Although gene expression during diapause termination in Ostrinia is similar to that found previously in flies, nominated genes for shifts in timing are species specific. Hence, across distant relatives the evolution of insect seasonality appears to involve unique genetic switches that direct organisms into distinct phases of the diapause pathway through wholesale restructuring of conserved gene regulatory networks.

A combination of sexual and ecological divergence contributes to rearrangement spread during initial stages of speciation

“…PCR primers for Z chromosome loci distributed across the chromosome were designed from the silkworm ( Bombyx mori ) Z chromosome and from ECB transcriptome sequences (Levy et al . ; Wadsworth & Dopman ; Wadsworth et al . ).…”

“…The second reference used four de novo transcriptomes that were previously constructed in ECB (Al‐Wathiqui et al . ; Wadsworth & Dopman ; N. Al‐Wathiqui, S. M. Lewis, E. B. Dopman, in prep; R. C. Levy, G. M. Kozak, E. B. Dopman, in prep.). Transcriptome data expanded our sequence coverage across the Z chromosome in the absence of a published genome.…”

Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

“…In D. melanogaster, wg, a gene in the multi-member wnt family, sits at the head of the so-called 'canonical' and calcium-dependent Wnt signaling pathways that play a central role throughout embryogenesis and morphogenesis (Wodarz and Nusse, 1998). Various studies of diapause developmental arrest implicate downregulation of the wnt-related pathways as either a regulator or result of the cessation of cell differentiation and proliferation (Wadsworth and Dopman, 2015;Wodarz and Nusse, 1998). In R. pomonella, calcium-dependent Wnt signaling is up-regulated 1 week after transfer from 4 to 23°C, suggesting a regulatory role upstream of pupal-adult apolysis and adult morphogenesis (Ragland et al, 2011).…”

“…Photoperiodic responses can be readily manipulated in the lab, and numerous physiological and genetic studies have identified candidate genes and mechanisms that may transduce photoperiodic signals upstream and downstream of major hormonal cues (Emerson et al, 2010;Poelchau et al, 2013;Poupardin et al, 2015;Schmidt et al, 2008;Sim and Denlinger, 2008;Tauber et al, 2007;Wadsworth and Dopman, 2015;Williams et al, 2006). In contrast, it has been more difficult to experimentally manipulate temperature effects because the sensitivity of development to thermal conditions often changes over the course of diapause (Hodek and Hodkova, 1988).…”

The genetic architecture underlying diapause termination in a planktonic crustacean

“…While the circadian clock gene timeless was not located in any of the detected QTLs, it was shown to epistatically interact with one of the QTLs detected by Mathias et al (). In contrast, differences in the seasonal diapause termination between two North American strains of the European Corn Borer Ostrinia nubilalis are controlled by a single, sex‐linked QTL pointing to a large genomic inversion harbouring multiple genes, including circadian clock genes (Dopman, Pérez, Bogdanowicz, & Harrison, ; Wadsworth & Dopman, ). A similar sex‐chromosome located locus is also associated diapause termination timing in swallowtail butterflies (Kunte et al, ).…”