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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)...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6138418/ https://www.ncbi.nlm.nih.gov/pubmed/30180162 http://dx.doi.org/10.1371/journal.pgen.1007612 |
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author | Yang, Yong Edery, Isaac |
author_facet | Yang, Yong Edery, Isaac |
author_sort | Yang, Yong |
collection | PubMed |
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. |
format | Online Article Text |
id | pubmed-6138418 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-61384182018-09-27 Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection Yang, Yong Edery, Isaac PLoS Genet Research Article 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. Public Library of Science 2018-09-04 /pmc/articles/PMC6138418/ /pubmed/30180162 http://dx.doi.org/10.1371/journal.pgen.1007612 Text en © 2018 Yang, Edery http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Yang, Yong Edery, Isaac Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection |
title | 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_short | 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 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6138418/ https://www.ncbi.nlm.nih.gov/pubmed/30180162 http://dx.doi.org/10.1371/journal.pgen.1007612 |
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