Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.

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)...

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Main Authors: Yong Yang, Isaac Edery
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-09-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC6138418?pdf=render
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spelling doaj-3ea9328683ba4723b260172d8f1d170c2020-11-25T01:19:27ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042018-09-01149e100761210.1371/journal.pgen.1007612Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.Yong YangIsaac EderySimilar 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.http://europepmc.org/articles/PMC6138418?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yong Yang
Isaac Edery
spellingShingle Yong Yang
Isaac Edery
Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
PLoS Genetics
author_facet Yong Yang
Isaac Edery
author_sort Yong Yang
title Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
title_short Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
title_full Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
title_fullStr Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
title_full_unstemmed Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
title_sort parallel clinal variation in the mid-day siesta of drosophila melanogaster implicates continent-specific targets of natural selection.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2018-09-01
description 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.
url http://europepmc.org/articles/PMC6138418?pdf=render
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