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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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Geographic variation in sunrise anticipation. Percentage of maximal activity across time (= late night activity level) was a normalization of each line’s activity profile between 0 and 1. The data were then averaged over lines for each population. R-squares were obtained at each circadian timepoint from the regression of population mean activity levels over latitude.
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Fig4: Geographic variation in sunrise anticipation. Percentage of maximal activity across time (= late night activity level) was a normalization of each line’s activity profile between 0 and 1. The data were then averaged over lines for each population. R-squares were obtained at each circadian timepoint from the regression of population mean activity levels over latitude.

Mentions: Population average locomotor activity patterns (Figure 1) suggest that the few hours preceding the morning light transition also exhibit geographic variation. In particular, the phase of the morning peak (around ZT00) of the Rhode Island (RI) population occurs before light transition whereas it occurs after light transition for Panama City (PC), (with Maine (ME), Virginia (VA) and Florida (FL) being intermediate), which would be consistent with genetic variation in the anticipation of sunrise. To investigate this hypothesis, we quantified ramping in activity relative to the nighttime maximum locomotor activity (Figure 4 and see material and methods normalization details). This analysis revealed substantial geographic variation for ramping activity. For example, at ZT23 the PC population had reached only 50% of maximal activity, whereas flies from northern latitudes were already at 75% of their maximum activity; latitude explains 83% of the variation in late night activity level at this timepoint (regression; p-value = 0.026).Figure 4


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)

Geographic variation in sunrise anticipation. Percentage of maximal activity across time (= late night activity level) was a normalization of each line’s activity profile between 0 and 1. The data were then averaged over lines for each population. R-squares were obtained at each circadian timepoint from the regression of population mean activity levels over latitude.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Geographic variation in sunrise anticipation. Percentage of maximal activity across time (= late night activity level) was a normalization of each line’s activity profile between 0 and 1. The data were then averaged over lines for each population. R-squares were obtained at each circadian timepoint from the regression of population mean activity levels over latitude.
Mentions: Population average locomotor activity patterns (Figure 1) suggest that the few hours preceding the morning light transition also exhibit geographic variation. In particular, the phase of the morning peak (around ZT00) of the Rhode Island (RI) population occurs before light transition whereas it occurs after light transition for Panama City (PC), (with Maine (ME), Virginia (VA) and Florida (FL) being intermediate), which would be consistent with genetic variation in the anticipation of sunrise. To investigate this hypothesis, we quantified ramping in activity relative to the nighttime maximum locomotor activity (Figure 4 and see material and methods normalization details). This analysis revealed substantial geographic variation for ramping activity. For example, at ZT23 the PC population had reached only 50% of maximal activity, whereas flies from northern latitudes were already at 75% of their maximum activity; latitude explains 83% of the variation in late night activity level at this timepoint (regression; p-value = 0.026).Figure 4

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
Related in: MedlinePlus