Abstract
Similar to many diurnal animals, Drosophila melanogaster exhibits a mid-day siesta that is more robust as ambient temperature rises, an adaptive response aimed at minimizing exposure to heat. Mid-day siesta levels are partly regulated by the thermosensitive splicing of a small intron (termed dmpi8) found in the 3’ untranslated region (UTR) of the circadian clock gene period (per). Using the well-studied D. melanogaster latitudinal cline along the eastern coast of Australia, we show that flies from temperate populations sleep less during the day compared to those from tropical regions. We identified combinations of four single nucleotide polymorphisms (SNPs) in the 3’ UTR of per that yield several different haplotypes. The two most abundant of these haplotypes exhibit a reciprocal tropical-temperate distribution in relative frequency. Intriguingly, transgenic flies with the major tropical isoform manifest increased daytime sleep and reduced dmpi8 splicing compared to those carrying the temperate variant. Our results strongly suggest that for a major portion of D. melanogaster in Australia, thermal adaptation of daily sleep behavior included spatially varying selection on ancestrally derived polymorphisms in the per 3’ UTR that differentially control dmpi8 splicing efficiency. Prior work showed that African flies from high altitudes manifest reduced mid-day siesta levels, indicative of parallel latitudinal and altitudinal adaptation across continents. However, geographical variation in per 3’ UTR haplotypes was not observed for African flies, providing a compelling case for inter-continental variation in factors targeted by natural selection in attaining a parallel adaptation. We propose that the ability to calibrate mid-day siesta levels to better match local temperature ranges is a key adaptation contributing to the successful colonization of D. melanogaster beyond its ancestral range in the lowlands of Sub-Saharan Africa.
Highlights
Wake-sleep cycles in animals are partially governed by interacting networks of cell-based circadian ‘clocks’ or pacemakers located in the brain, in addition to sleep homeostatic and arousal pathways
Latitudinal adaptation of mid-day siesta they have a less pronounced siesta? we show that in the common fruit fly, Drosophila melanogaster, those from temperate regions in Australia exhibit less mid-day siesta compared to their tropical counterparts
The results suggest that selection for increased dmpi8 splicing efficiency played a major role in the thermal adaptation of African flies to the cooler climates found at high altitudes
Summary
Wake-sleep cycles in animals are partially governed by interacting networks of cell-based circadian (ffi hr) ‘clocks’ or pacemakers located in the brain, in addition to sleep homeostatic and arousal pathways. Increases in average daily temperature are accompanied by a gradual delay in the onset of the evening bout of activity and a more prolonged mid-day siesta [7], presumably an adaptive response that minimizes the risks associated with exposure to the hot mid-day sun This thermal plasticity in daily behavior is partially controlled by the thermosensitive splicing of an intron in the 3’ untranslated region (UTR) of the D. melanogaster period (dper) transcript [7, 8], which is the key circadian clock factor regulating the pace of the clock [9]. While nighttime sleep levels are generally less affected by dmpi splicing compared to daytime sleep, it follows the same trend in being less consolidated as dmpi splicing efficiency increases [11, 12]
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