Variation in thermal sensitivity of diapause development among individuals and over time predicts life history timing in a univoltine insect

Abstract

Physiological time is important for understanding the development and seasonal timing of ectothermic animals, but has largely been applied to developmental processes that occur during spring and summer such as morphogenesis. There is a substantial knowledge gap in the relationship between temperature and development during winter, a season that is increasingly impacted by climate change. Most temperate insects overwinter in diapause, a developmental process with little obvious morphological change. We used principles from the physiological time literature to measure and model the thermal sensitivity of diapause development rate in the apple maggot fly Rhagoletis pomonella, a univoltine fly whose diapause duration varies substantially within and among populations. We showed that diapause duration could be modelled with simple linear relationships between diapause development rate and temperature. Low temperatures were necessary for most individuals to complete diapause, similar to many insects. However, we also found evidence for an ontogenetic shift in the thermal sensitivity of diapause: diapause development proceeded more quickly at high temperatures later in diapause and in the absence of quiescence, a phenomenon not previously reported. Increasingly warmer temperatures during and after winter may impact the phenology of this and other insects with temperature-sensitive diapause, impacting their viability.

Overwintering strategy regulates phenological sensitivity and consequences for ecological services in a clade of temperate North American insects

“…For pupal overwinterers, a temporal trend towards later adult onset, opposite that seen in egg overwinters, dampened environment‐related phenological advances. This trend may indicate shifts towards suboptimal winter temperatures not captured by our winter metrics, affecting diapause termination and post‐diapause development (Lehmann et al., 2017; Toxopeus et al., 2023). Larval overwinterers are the only group who don't exhibit strong temporal shifts after accounting for environmental effects.…”

Conserved cold tolerance ofRhagoletisspecies from different host fruits, elevations in Colorado, USA

“…This relationship is maintained even when apple and hawthorn populations are overwintered under common conditions in the laboratory (Feder et al, 1993; Smith, 1988) and is driving speciation between sympatric populations of apple- and hawthorn-infesting R. pomonella (Dowle et al, 2020; Filchak et al, 2000; Ragland et al, 2017). The duration of cold exposure also impacts developmental timing, with longer chilling of pupae resulting in faster completion of post-chill eclosion, with apple flies eclosing faster than hawthorn flies (Dambroski and Feder, 2007; Feder et al, 1997; Toxopeus et al, 2023; Yee et al, 2023). We have recently observed Rhagoletis flies infesting introduced (non-native) crabapple with fruiting phenology that overlaps with sympatric hawthorn trees (see Methods), providing an opportunity to examine the impact of a rare host fruit on R. pomonella life history timing and cold tolerance.…”