Abstract
BackgroundMany diurnal animals exhibit a mid-day ‘siesta’, generally thought to be an adaptive response aimed at minimizing exposure to heat on warm days, suggesting that in regions with cooler climates mid-day siestas might be a less prominent feature of animal behavior. Drosophila melanogaster exhibits thermal plasticity in its mid-day siesta that is partly governed by the thermosensitive splicing of the 3’-terminal intron (termed dmpi8) from the key circadian clock gene period (per). For example, decreases in temperature lead to progressively more efficient splicing, which increasingly favors activity over sleep during the mid-day. In this study we sought to determine if the adaptation of D. melanogaster from its ancestral range in the lowlands of tropical Africa to the cooler temperatures found at high altitudes involved changes in mid-day sleep behavior and/or dmpi8 splicing efficiency.ResultsUsing natural populations of Drosophila melanogaster from different altitudes in tropical Africa we show that flies from high elevations have a reduced mid-day siesta and less consolidated sleep. We identified a single nucleotide polymorphism (SNP) in the per 3’ untranslated region that has strong effects on dmpi8 splicing and mid-day sleep levels in both low and high altitude flies. Intriguingly, high altitude flies with a particular variant of this SNP exhibit increased dmpi8 splicing efficiency compared to their low altitude counterparts, consistent with reduced mid-day siesta. Thus, a boost in dmpi8 splicing efficiency appears to have played a prominent but not universal role in how African flies adapted to the cooler temperatures at high altitude.ConclusionsOur findings point towards mid-day sleep behavior as a key evolutionary target in the thermal adaptation of animals, and provide a genetic framework for investigating daytime sleep in diurnal animals which appears to be driven by mechanisms distinct from those underlying nighttime sleep.
Highlights
Many diurnal animals exhibit a mid-day ‘siesta’, generally thought to be an adaptive response aimed at minimizing exposure to heat on warm days, suggesting that in regions with cooler climates mid-day siestas might be a less prominent feature of animal behavior
The majority of the findings presented in this report are based on flies from Cameroon and Kenya because for both countries numerous independent lines from relatively low and high altitudes were available—prior studies have used even less extreme altitude ranges used here for defining low and high altitude groups for D. melanogaster from sub-Saharan Africa; e.g., [31]
In summary, we show that natural populations of D. melanogaster from tropical Africa living at high altitudes exhibit significantly reduced mid-day sleep levels and generally more fragmented sleep compared to their lowland counterparts
Summary
Many diurnal animals exhibit a mid-day ‘siesta’, generally thought to be an adaptive response aimed at minimizing exposure to heat on warm days, suggesting that in regions with cooler climates mid-day siestas might be a less prominent feature of animal behavior. D. melanogaster manifest a longer and more robust mid-day siesta, delayed and more nocturnal evening activity bout, and less dramatic an earlier offset in the morning bout of activity [4] We showed that this behavioral plasticity is partly governed by the thermal sensitive splicing of the 3’-terminal intron found in the key circadian clock gene termed period (per) [4, 17, 18]. Splicing of this intron (called dmpi; D. melanogaster per intron 8) is progressively more efficient as daily temperatures decrease, leading to an increase in per mRNA levels [4]. The mid-day siesta in D. melanogaster is very sensitive to being shaped by thermal cues
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