Genome-wide variation and transcriptional changes in diverse developmental processes underlie the rapid evolution of seasonal adaptation

Abstract

Many organisms enter a dormant state in their life cycle to deal with predictable changes in environments over the course of a year. The timing of dormancy is therefore a key seasonal adaptation, and it evolves rapidly with changing environments. We tested the hypothesis that differences in the timing of seasonal activity are driven by differences in the rate of development during diapause in Rhagoletis pomonella, a fly specialized to feed on fruits of seasonally limited host plants. Transcriptomes from the central nervous system across a time series during diapause show consistent and progressive changes in transcripts participating in diverse developmental processes, despite a lack of gross morphological change. Moreover, population genomic analyses suggested that many genes of small effect enriched in developmental functional categories underlie variation in dormancy timing and overlap with gene sets associated with development rate in Drosophila melanogaster. Our transcriptional data also suggested that a recent evolutionary shift from a seasonally late to a seasonally early host plant drove more rapid development during diapause in the early fly population. Moreover, genetic variants that diverged during the evolutionary shift were also enriched in putative cis regulatory regions of genes differentially expressed during diapause development. Overall, our data suggest polygenic variation in the rate of developmental progression during diapause contributes to the evolution of seasonality in R. pomonella. We further discuss patterns that suggest hourglass-like developmental divergence early and late in diapause development and an important role for hub genes in the evolution of transcriptional divergence.

A unifying, eco‐physiological framework for animal dormancy

“…To overcome this challenge, insect physiologists divided deep, programmed dormancy into a set of eco‐physiological phases, which describe sequential modifications to physiology and behaviour that insects undergo during transitions into and out of dormancy (Danks, 1987; Koštál, 2006). Experimental transcriptomic studies support the biological relevance of these phases (Dowle et al., 2020; Koštál et al., 2017). With this utility in mind, our phases of dormancy build on those defined by Koštál (2006) and expand their utility to all animals.…”

“…Experimental transcriptomic studies support the biological relevance of these phases (Dowle et al, 2020;Koštál et al, 2017). With this utility in mind, our phases of dormancy build on those defined by Koštál (2006) and expand their utility to all animals.…”

“…In most cases, the mechanisms underlying metabolic suppression are still an open question and active field of research (Hand et al., 2011; Mathers & Staples, 2019). The cell cycle is arrested leading to a cessation of growth and development (Carey et al., 2003; Dowle et al., 2020; Hand et al., 2016).…”

“…The potentiation phase includes the period over which the endogenous lock on development and activity is gradually released, until active season behaviour resumes. The mechanisms by which the endogenous lock is released is an active research area in both insect and mammal fields (Dowle et al., 2020; Hut et al., 2014; Meyers et al., 2016).…”

“…In insects, transcriptomic work suggests that metabolism and cellular growth/proliferation are up‐regulated together before morphogenesis, growth and development; however, some of the regulatory differences leading to activation must begin in an earlier phase (i.e. during potentiation; Dowle et al., 2020; Meyers et al., 2016; Ragland et al., 2011). Similarly, we know that the same neuroendocrine systems are involved in both the inhibition and activation of reproduction in mammals as part of the dormancy program, but the connections between these systems differ between preparation/initiation and potentiation/activation (Dardente et al., 2014; Follett, 2015; Hut et al., 2014).…”