A hormetic model of rapid cold hardening in Drosophila melanogaster reveals threshold effects on survival and low fertility resilience

Abstract

Variable thermal environments may have both detrimental and beneficial effects. For example, extreme temperatures may challenge homeostasis and inflict tissue damage but may also induce acclimation that improves stress resilience. Hormetic models provide a framework to understand dosage-dependent, contrasting beneficial and detrimental effects from physiological and ecological perspectives. We used a hormetic framework and associated quantitative models to investigate how a range of relatively cold, pre-exposure temperatures influence survival and fertility following cold shock at a more extreme cold temperature in the fruit fly Drosophila melanogaster. Cold pre-exposure can induce a protective rapid cold hardening (RCH) response, fail to stimulate a response, or cause direct cold injury. We found a plateau-shaped relationship between pre-exposure temperature and female survival resilience, where survival following a cold shock remains high across a range of temperatures, with sharp transitions at higher and lower temperatures. Bayesian fitting of a bi-logistic model highlights these transitions at temperature thresholds that govern processes mediating both acclimation and cold injury. In contrast to survival, female fertility resilience exhibited a muted response to pre-exposure temperature in the presence and absence of post-stress mating opportunities. Overall, a range of pre-exposure temperatures allowed low but successful reproduction following cold shock. High survival but low fertility resilience is consistent with a) differential impacts of cold on somatic and reproductive tissues and b) a growing body of literature suggesting that the thermal sensitivity of fertility may be more limiting than survival for population persistence in variable and changing climates. Summary statementA hormetic model shows how sharp temperature thresholds govern beneficial rapid cold hardening and detrimental cold injury that have well-defined effects on survival, but only weakly affect fertility.