Is diapause an ancient adaptation in Drosophila?

[Display omitted] •Diapause in cosmopolitan D. melanogaster and D. simulans is photoperiodic in temperate regions.•Winter/spring simulations enhance the diapause response of D. melanogaster but not D. simulans.•As in robustly diapausing species sugar metabolism changes during D. melanogaster diapause.•Tropical species exhibit diapause suggesting it is ancestral and evolved as a stress response.•Contradictory results among studies are largely resolved by considering how diapause is scored. D. melanogaster enters a state of reproductive arrest when exposed to low temperatures (12°C) and shorter photoperiods. A number of studies have suggested that diapause has recently evolved in European D. melanogaster populations, that it is not present in the sibling species D. simulans, that it is non-photoperiodic in American D. melanogaster populations, and that it spontaneously terminates after 6–8weeks. We have studied the overwintering phenotype under different conditions and observe that American, European and, surprisingly, African D. melanogaster populations can show photoperiodic diapause, as can European, but not African D. simulans. Surprisingly other Drosophila species from pan-tropical regions can also show significant levels of photoperiodic diapause. We observe that spontaneous termination of diapause after a few weeks can be largely avoided with a more realistic winter simulation for D. melanogaster, but not D. simulans. Examining metabolite accumulation during diapause reveals that the shallow diapause of D. melanogaster has similar features to that of other more robustly-diapausing species. Our results suggest that diapause may be an ancient character that emerged in the tropics to resist unfavourable seasonal conditions and which has been enhanced during D. melanogaster’s colonisation of temperate regions. Our results also highlight how different methodologies to quantify diapause can lead to apparently conflicting results that we believe can now largely be resolved.