Costs of averting or prematurely terminating diapause associated with slow decline of metabolic rates at low temperature.

Diapause, a form of insect dormancy, generally facilitates overwintering by increasing cold tolerance and decreasing energy drain at high temperatures via metabolic rate suppression. Averting or terminating diapause prior to winter is generally assumed to be a lethal phenotype. However, low temperature acclimation can also increase cold tolerance and decrease metabolic rates. Here, we tested the hypothesis that non- and post-diapause individuals in a cold-induced quiescence can achieve a diapause-like phenotype, compensating for the potential costs of averting diapause. We tested this in the apple maggot fly Rhagoletis pomonella, which typically overwinters in the soil as a diapause pupa, but can avert diapause (non-diapause) or terminate diapause early ('weak diapause') when reared at warm temperatures. Metabolic rates were initially higher in non- and post-diapause than diapause pupae at high (25 °C) and low (4 °C) temperatures, but quiescent non- and post-diapause pupae achieved diapause-like metabolic rates slowly over time when incubated at 4 °C for several weeks. We found that diapause and quiescent pupae were freeze-avoidant and had similar tolerance of extreme low temperatures (cooling to c. -18 °C) following 8 weeks acclimation at 4 °C. Despite high tolerance of subzero temperatures, quiescent pupae did not survive well when chilled for prolonged periods (8 weeks or more) at 4 °C. We conclude that cold acclimation can only partially compensate for costs associated with aversion or premature termination of diapause, and that energy drain at low (not just high) temperatures likely contributes to chilling mortality in quiescent insects.