One phase of the dormancy developmental pathway is critical for the evolution of insect seasonality

Abstract

Evolutionary change in the timing of dormancy enables animals and plants to adapt to changing seasonal environments and can result in ecological speciation. Despite its clear biological importance, the mechanisms underlying the evolution of dormancy timing in animals remain poorly understood because of a lack of anatomical landmarks to discern which phase of dormancy an individual is experiencing. Taking advantage of the nearly universal characteristic of metabolic suppression during insect dormancy (diapause), we use patterns of respiratory metabolism to document physiological landmarks of dormancy and test which of the distinct phases of the dormancy developmental pathway contribute to a month-long shift in diapause timing between a pair of incipient moth species. Here, we show that divergence in life cycle between the earlier-emerging E-strain and the later-emerging Z-strain of European corn borer (ECB) is clearly explained by a delay in the timing of the developmental transition from the diapause maintenance phase to the termination phase. Along with recent findings indicating that life-cycle differences between ECB strains stem from allelic variation at a single sex-linked locus, our results demonstrate how dramatic shifts in animal seasonality can result from simple developmental and genetic changes. Although characterizing the multiple phases of the diapause developmental programme in other locally adapted populations and species will undoubtedly yield surprises about the nature of animal dormancy, results in the ECB moth suggest that focusing on genetic variation in the timing of the dormancy termination phase may help explain how (or whether) organisms rapidly respond to global climate change, expand their ranges after accidental or managed introductions, undergo seasonal adaptation, or evolve into distinct species through allochronic isolation.

Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines

“…The pattern is similar to what has previously been observed for the European corn borer (Wadsworth et al. 2013) and the apple maggot fly (Ragland et al. 2011).…”

A recombination suppressor contributes to ecological speciation in OSTRINIA moths

“…A subset of Z × E backcross offspring was mapped for a major sex-linked factor (named Pdd) controlling diapause emergence time (Glover et al, 1992;Dopman et al, 2005), defined as the time to pupation for over-wintering caterpillars under environmental conditions conducive to breaking diapause. Differences at Pdd contribute to temporal isolation between Z and E strains in North America by conferring an~30-day shift in emergence and thus adult-mating flights (Wadsworth et al, 2013). Shifts in adult flights between univoltine Z and bivoltine E populations eliminate as much as 85% gene flow in nature (Dopman et al, 2010).…”

Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

“…After 35 days of exposure to these conditions, diapausing borers remain at the 5th instar whereas direct developing insects will have already pupated or enclosed as adults (Glover et al, 1992;Dopman et al, 2005;Wadsworth et al, 2013). Diapause was terminated in 36-day-old larvae using long-day conditions (16:8 LD at 26°C) (Glover et al, 1992;Dopman et al, 2005;Wadsworth et al, 2013). Alternative developmental genetic pathways underlying differences in diapause termination timing seem to be triggered by Pdd within the first 7 days after insects experience diapausebreaking cues, as indicated by elevated respiratory metabolism in the Estrain but not the Z-strain (Wadsworth et al, 2013).…”

“…After 35 days of exposure to these conditions, diapausing borers remain at the 5th instar whereas direct developing insects will have already pupated or enclosed as adults (Glover et al, 1992;Dopman et al, 2005;Wadsworth et al, 2013). Diapause was terminated in 36-day-old larvae using long-day conditions (16:8 LD at 26°C) (Glover et al, 1992;Dopman et al, 2005;Wadsworth et al, 2013).…”

“…1A) (Wadsworth et al, 2013). Within a week of exposure to diapausebreaking (long-day) conditions, E-strain moths rapidly progress through the diapause termination phase and enter post-diapause development, as indicated by increased respiratory metabolism.…”