Strong Costs and Benefits of Winter Acclimatization in Drosophila melanogaster

Abstract

Studies on thermal acclimation in insects are often performed on animals acclimated in the laboratory under conditions that are not ecologically relevant. Costs and benefits of acclimation responses under such conditions may not reflect costs and benefits in natural populations subjected to daily and seasonal temperature fluctuations. Here we estimated costs and benefits in thermal tolerance limits in relation to winter acclimatization of Drosophila melanogaster. We sampled flies from a natural habitat during winter in Denmark (field flies) and compared heat and cold tolerance of these to that of flies collected from the same natural population, but acclimated to 25 °C or 13 °C in the laboratory (laboratory flies). We further obtained thermal performance curves for egg-to-adult viability of field and laboratory (25 °C) flies, to estimate possible cross-generational effects of acclimation. We found much higher cold tolerance and a lowered heat tolerance in field flies compared to laboratory flies reared at 25 °C. Flies reared in the laboratory at 13 °C exhibited the same thermal cost-benefit relations as the winter acclimatized flies. We also found a cost of winter acclimatization in terms of decreased egg-to-adult viability at high temperatures of eggs laid by winter acclimatized flies. Based on our findings we suggest that winter acclimatization in nature can induce strong benefits in terms of increased cold tolerance. These benefits can be reproduced in the laboratory under ecologically relevant rearing and testing conditions, and should be incorporated in species distribution modelling. Winter acclimatization also leads to decreased heat tolerance. This may create a mismatch between acclimation responses and the thermal environment, e.g. if temperatures suddenly increase during spring, under current and expected more variable future climatic conditions.

Proteomic data reveals a physiological basis for costs and benefits associated with thermal acclimation

“…1). These results are in accordance with other studies showing marked benefits and costs across tolerances with thermal acclimation (Chidawanyika and Terblanche, 2011;Chown and Terblanche, 2006;Kristensen et al, 2008;Loeschcke and Hoffmann, 2007;Schou et al, 2015). Consequences of climate change include higher and more variable temperatures in many parts of the world (IPCC, 2013).…”

“…Consequences of climate change include higher and more variable temperatures in many parts of the world (IPCC, 2013). Thus the strong trade-off between tolerances observed here and in other studies clearly suggests that thermal fluctuation constitutes a challenge to ectotherms in nature (Kristensen et al, 2008;Schou et al, 2015) and will potentially be even more of a challenge in the predicted future thermal environment. Fig.…”

“…4). In temperate climates, D. melanogaster is known to survive winters in the adult state, where they are often exposed to temperatures below 10°C for several months (Izequierdo, 1991;Schou et al, 2015), resulting in a longer lifespan (Miquel et al, 1976). This suggests fundamental differences in the type of stress induced by 12°C and 31°C, which is supported by the proteomic data (Figs 2-4 and Table S1).…”

“…Egg-to-adult viability was modelled with a logistic regression, and because D. melanogaster has a quadratic performance curve for this trait (e.g. Schou et al, 2015), temperature was modelled as such. We observed overdispersion in the model and corrected the standard errors using a quasigeneralized linear model (Zuur et al, 2009).…”

“…However, in their natural habitats, Drosophila melanogaster and other ectotherms are exposed to thermal stress for extended periods e.g. during cold winters or hot summers (Izequierdo, 1991;Rodríguez-Trelles et al, 2013;Schou et al, 2015), making the molecular consequences of longterm exposure of different life stages highly ecologically relevant.…”