Abstract

BackgroundDrosophila melanogaster often shows correlations between latitude and phenotypic or genetic variation on different continents, which suggests local adaptation with respect to a heterogeneous environment. Previous phenotypic analyses of latitudinal clines have investigated mainly physiological, morphological, or life-history traits. Here, we studied latitudinal variation in sleep in D. melanogaster populations from North and Central America. In parallel, we used RNA-seq to identify interpopulation gene expression differences.ResultsWe found that in D. melanogaster the average nighttime sleep bout duration exhibits a latitudinal cline such that sleep bouts of equatorial populations are roughly twice as long as those of temperate populations. Interestingly, this pattern of latitudinal variation is not observed for any daytime measure of activity or sleep. We also found evidence for geographic variation for sunrise anticipation. Our RNA-seq experiment carried out on heads from a low and high latitude population identified a large number of gene expression differences, most of which were time dependent. Differentially expressed genes were enriched in circadian regulated genes and enriched in genes potentially under spatially varying selection.ConclusionOur results are consistent with a mechanistic and selective decoupling of nighttime and daytime activity. Furthermore, the present study suggests that natural selection plays a major role in generating transcriptomic variation associated with circadian behaviors. Finally, we identified genomic variants plausibly causally associated with the observed behavioral and transcriptomic variation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0316-2) contains supplementary material, which is available to authorized users.

Highlights

  • Drosophila melanogaster often shows correlations between latitude and phenotypic or genetic variation on different continents, which suggests local adaptation with respect to a heterogeneous environment

  • D. melanogaster males sampled from populations collected along a latitudinal gradient ranging from Maine (USA; 44°N) to Panama City (Panama; 8°N) were entrained under semi-natural conditions prior to measurement of their locomotor activity

  • The observation that nighttime walking speed shows no evidence of latitudinal variation (Figure 2E and F) supports the idea that sleep, rather than walking speed, constitutes the key behavioral difference in nighttime activity levels in higher vs. lower latitude populations

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Summary

Introduction

Drosophila melanogaster often shows correlations between latitude and phenotypic or genetic variation on different continents, which suggests local adaptation with respect to a heterogeneous environment. Latitudinal clines have been of particular interest because many organisms and traits show patterns of geographic variation consistent with locally varying selective forces correlated with latitude [2]. In the model species Drosophila melanogaster, numerous phenotypic traits (reviewed in [3]), including some related to circadian behaviors [4] are correlated with latitude suggesting they are shaped by spatially varying selection. Despite their connection to circadian and locomotor activity rhythms, the population processes. Our analysis of the head transcriptome for the two populations showing the greatest sleep differences revealed that most gene expression differences between populations are circadian-time dependent and provided potentially valuable molecular insights into the observed behavioral phenotypes

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