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Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila

Resolving the role of natural selection is a basic objective of evolutionary biology. It is generally difficult to detect the influence of selection because ubiquitous non-selective stochastic change in allele frequencies (genetic drift) degrades evidence of selection. As a result, selection scans t...

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Autor principal: Bertram, Jason
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8509871/
https://www.ncbi.nlm.nih.gov/pubmed/34591854
http://dx.doi.org/10.1371/journal.pgen.1009833
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author Bertram, Jason
author_facet Bertram, Jason
author_sort Bertram, Jason
collection PubMed
description Resolving the role of natural selection is a basic objective of evolutionary biology. It is generally difficult to detect the influence of selection because ubiquitous non-selective stochastic change in allele frequencies (genetic drift) degrades evidence of selection. As a result, selection scans typically only identify genomic regions that have undergone episodes of intense selection. Yet it seems likely such episodes are the exception; the norm is more likely to involve subtle, concurrent selective changes at a large number of loci. We develop a new theoretical approach that uncovers a previously undocumented genome-wide signature of selection in the collective divergence of allele frequencies over time. Applying our approach to temporally resolved allele frequency measurements from laboratory and wild Drosophila populations, we quantify the selective contribution to allele frequency divergence and find that selection has substantial effects on much of the genome. We further quantify the magnitude of the total selection coefficient (a measure of the combined effects of direct and linked selection) at a typical polymorphic locus, and find this to be large (of order 1%) even though most mutations are not directly under selection. We find that selective allele frequency divergence is substantially elevated at intermediate allele frequencies, which we argue is most parsimoniously explained by positive—not negative—selection. Thus, in these populations most mutations are far from evolving neutrally in the short term (tens of generations), including mutations with neutral fitness effects, and the result cannot be explained simply as an ongoing purging of deleterious mutations.
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spelling pubmed-85098712021-10-13 Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila Bertram, Jason PLoS Genet Research Article Resolving the role of natural selection is a basic objective of evolutionary biology. It is generally difficult to detect the influence of selection because ubiquitous non-selective stochastic change in allele frequencies (genetic drift) degrades evidence of selection. As a result, selection scans typically only identify genomic regions that have undergone episodes of intense selection. Yet it seems likely such episodes are the exception; the norm is more likely to involve subtle, concurrent selective changes at a large number of loci. We develop a new theoretical approach that uncovers a previously undocumented genome-wide signature of selection in the collective divergence of allele frequencies over time. Applying our approach to temporally resolved allele frequency measurements from laboratory and wild Drosophila populations, we quantify the selective contribution to allele frequency divergence and find that selection has substantial effects on much of the genome. We further quantify the magnitude of the total selection coefficient (a measure of the combined effects of direct and linked selection) at a typical polymorphic locus, and find this to be large (of order 1%) even though most mutations are not directly under selection. We find that selective allele frequency divergence is substantially elevated at intermediate allele frequencies, which we argue is most parsimoniously explained by positive—not negative—selection. Thus, in these populations most mutations are far from evolving neutrally in the short term (tens of generations), including mutations with neutral fitness effects, and the result cannot be explained simply as an ongoing purging of deleterious mutations. Public Library of Science 2021-09-30 /pmc/articles/PMC8509871/ /pubmed/34591854 http://dx.doi.org/10.1371/journal.pgen.1009833 Text en © 2021 Jason Bertram https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Bertram, Jason
Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila
title Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila
title_full Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila
title_fullStr Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila
title_full_unstemmed Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila
title_short Allele frequency divergence reveals ubiquitous influence of positive selection in Drosophila
title_sort allele frequency divergence reveals ubiquitous influence of positive selection in drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8509871/
https://www.ncbi.nlm.nih.gov/pubmed/34591854
http://dx.doi.org/10.1371/journal.pgen.1009833
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