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Evidence that natural selection maintains genetic variation for sleep in Drosophila melanogaster.

Svetec N, Zhao L, Saelao P, Chiu JC, Begun DJ - BMC Evol. Biol. (2015)

Bottom Line: We also found evidence for geographic variation for sunrise anticipation.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolution and Ecology, University of California, 3352 Storer Hall, One Shields Ave., Davis, CA, 95618, USA. nhsvetec@ucdavis.edu.

ABSTRACT

Background: 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. 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.

Results: We 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.

Conclusion: Our 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.

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Variation in the direction of the expression difference. The figure shows the number of genes significantly overexpressed in PC vs. RI (blue) and RI vs. PC (red) for each timepoint.
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Fig6: Variation in the direction of the expression difference. The figure shows the number of genes significantly overexpressed in PC vs. RI (blue) and RI vs. PC (red) for each timepoint.

Mentions: At ZT01 there is no obvious pattern of greater transcript abundance being more common in one population or the other (Figure 6), though the magnitude of expression difference between populations is greater for genes expressed at a higher level in RI compared to genes expressed at a higher level in PC (average fold change for RI = 2.47; for PC = 1.42; MW test: p < 0.0001). The remaining timepoints, all of which are nighttime, show a different pattern (Figure 6), with a greater proportion of differentially expressed genes showing higher mRNA abundance in RI than in PC. Thus, it appears that population differences in transcriptional activity show some degree of correlation with population differences in nighttime activity. This is consistent with previous gene expression analyses showing that transcription levels in Drosophila heads are higher in awake vs. sleeping individuals [27].Figure 6


Evidence that natural selection maintains genetic variation for sleep in Drosophila melanogaster.

Svetec N, Zhao L, Saelao P, Chiu JC, Begun DJ - BMC Evol. Biol. (2015)

Variation in the direction of the expression difference. The figure shows the number of genes significantly overexpressed in PC vs. RI (blue) and RI vs. PC (red) for each timepoint.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4374177&req=5

Fig6: Variation in the direction of the expression difference. The figure shows the number of genes significantly overexpressed in PC vs. RI (blue) and RI vs. PC (red) for each timepoint.
Mentions: At ZT01 there is no obvious pattern of greater transcript abundance being more common in one population or the other (Figure 6), though the magnitude of expression difference between populations is greater for genes expressed at a higher level in RI compared to genes expressed at a higher level in PC (average fold change for RI = 2.47; for PC = 1.42; MW test: p < 0.0001). The remaining timepoints, all of which are nighttime, show a different pattern (Figure 6), with a greater proportion of differentially expressed genes showing higher mRNA abundance in RI than in PC. Thus, it appears that population differences in transcriptional activity show some degree of correlation with population differences in nighttime activity. This is consistent with previous gene expression analyses showing that transcription levels in Drosophila heads are higher in awake vs. sleeping individuals [27].Figure 6

Bottom Line: We also found evidence for geographic variation for sunrise anticipation.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolution and Ecology, University of California, 3352 Storer Hall, One Shields Ave., Davis, CA, 95618, USA. nhsvetec@ucdavis.edu.

ABSTRACT

Background: 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. 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.

Results: We 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.

Conclusion: Our 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.

Show MeSH