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Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster

Chromosomal inversions are among the primary drivers of genome structure evolution in a wide range of natural populations. Although there is an impressive array of theory and empirical analyses that have identified conditions under which inversions can be positively selected, comparatively little da...

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Autores principales: McBroome, Jakob, Liang, David, Corbett-Detig, Russell
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7487137/
https://www.ncbi.nlm.nih.gov/pubmed/32437518
http://dx.doi.org/10.1093/gbe/evaa103
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author McBroome, Jakob
Liang, David
Corbett-Detig, Russell
author_facet McBroome, Jakob
Liang, David
Corbett-Detig, Russell
author_sort McBroome, Jakob
collection PubMed
description Chromosomal inversions are among the primary drivers of genome structure evolution in a wide range of natural populations. Although there is an impressive array of theory and empirical analyses that have identified conditions under which inversions can be positively selected, comparatively little data are available on the fitness impacts of these genome structural rearrangements themselves. Because inversion breakpoints can disrupt functional elements and alter chromatin domains, the precise positioning of an inversion’s breakpoints can strongly affect its fitness. Here, we compared the fine-scale distribution of low-frequency inversion breakpoints with those of high-frequency inversions and inversions that have gone to fixation between Drosophila species. We identified a number of differences among frequency classes that may influence inversion fitness. In particular, breakpoints that are proximal to insulator elements, generate large tandem duplications, and minimize impacts on gene coding spans which are more prevalent in high-frequency and fixed inversions than in rare inversions. The data suggest that natural selection acts to preserve both genes and larger cis-regulatory networks in the occurrence and spread of rearrangements. These factors may act to limit the availability of high-fitness arrangements when suppressed recombination is favorable.
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spelling pubmed-74871372020-09-16 Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster McBroome, Jakob Liang, David Corbett-Detig, Russell Genome Biol Evol Research Article Chromosomal inversions are among the primary drivers of genome structure evolution in a wide range of natural populations. Although there is an impressive array of theory and empirical analyses that have identified conditions under which inversions can be positively selected, comparatively little data are available on the fitness impacts of these genome structural rearrangements themselves. Because inversion breakpoints can disrupt functional elements and alter chromatin domains, the precise positioning of an inversion’s breakpoints can strongly affect its fitness. Here, we compared the fine-scale distribution of low-frequency inversion breakpoints with those of high-frequency inversions and inversions that have gone to fixation between Drosophila species. We identified a number of differences among frequency classes that may influence inversion fitness. In particular, breakpoints that are proximal to insulator elements, generate large tandem duplications, and minimize impacts on gene coding spans which are more prevalent in high-frequency and fixed inversions than in rare inversions. The data suggest that natural selection acts to preserve both genes and larger cis-regulatory networks in the occurrence and spread of rearrangements. These factors may act to limit the availability of high-fitness arrangements when suppressed recombination is favorable. Oxford University Press 2020-05-21 /pmc/articles/PMC7487137/ /pubmed/32437518 http://dx.doi.org/10.1093/gbe/evaa103 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
McBroome, Jakob
Liang, David
Corbett-Detig, Russell
Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster
title Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster
title_full Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster
title_fullStr Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster
title_full_unstemmed Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster
title_short Fine-Scale Position Effects Shape the Distribution of Inversion Breakpoints in Drosophila melanogaster
title_sort fine-scale position effects shape the distribution of inversion breakpoints in drosophila melanogaster
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7487137/
https://www.ncbi.nlm.nih.gov/pubmed/32437518
http://dx.doi.org/10.1093/gbe/evaa103
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