University of Western Ontario London, Ontario, Canada
Temperate insects spend over half their lives overwintering, during which most enter diapause; a programmed state of developmental arrest characterized by metabolic suppression. Metabolic suppression is a hallmark of diapause, yet we know little about the mechanisms underpinning this phenomenon in diapausing insects, or how suppression is reversed in the spring. In this study, we show that metabolic suppression during diapause in the Colorado potato beetle results from the break-down of flight muscle mitochondria via mitophagy. Diapausing Colorado potato beetles (Leptinotarsa decemlineata) suppress their metabolism by 90% in the winter, and this lowered metabolic rate coincides with a similar reduction in flight muscle mitochondrial function and density. During early diapause, beetles increase the expression of mitophagy-related transcripts in their flight muscle, which is coincident with an increase in the appearance of mitophagy-related structures in flight muscle cells. Knocking down the expression of a mitophagy-related transcript (Parkin) using RNAi prevented some mitochondrial breakdown and restored whole animal metabolic rate suggesting that this metabolic suppression is driven by mitophagy. As diapause ends, beetles reverse this mitophagy and activate mitochondrial biogenesis in their flight muscle to replenish their mitochondrial pools. This mitochondrial biogenesis is activated in anticipation of diapause termination, and in the absence of any external stimuli. Overall, our study shows a unique pattern by which beetles can regulate mitochondrial homeostasis to contribute to whole-animal shifts in energy metabolism. Because many other diapausing insects generate flight muscle during the winter, it is possible that re-modelling flight muscle mitochondrial homeostasis to save energy is a widespread strategy.
