Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

Most of the current knowledge on the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions annotated in the reference genome of Drosophila melanogaster, in 91 samples from 60 worldwide natural populations. We identified a set of 300 polymorphic TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Besides, we identified a set of 21 fixed TEs also likely to be adaptive. Indeed, we, and others, found evidence of selection for 84 of these reference TE insertions. The analysis of the genes located nearby these 84 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affects expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well.

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Main Authors: Rech, Gabriel E., Bogaerts-Márquez, María, Barrón, Maite G., Merenciano, Miriam, Villanueva-Cañas, José Luis, Horváth, Vivien, Fiston-Lavier, Anna-Sophie, Luyten, Isabelle, Venkataram, Sandeep, Quesneville, Hadi, Petrov, Dmitri A., González Pérez, Josefa
Other Authors: European Commission
Format: artículo biblioteca
Published: Public Library of Science 2019-02-19
Online Access:http://hdl.handle.net/10261/207488
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/100000002
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spelling dig-ibe-es-10261-2074882021-12-27T15:35:52Z Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila Rech, Gabriel E. Bogaerts-Márquez, María Barrón, Maite G. Merenciano, Miriam Villanueva-Cañas, José Luis Horváth, Vivien Fiston-Lavier, Anna-Sophie Luyten, Isabelle Venkataram, Sandeep Quesneville, Hadi Petrov, Dmitri A. González Pérez, Josefa European Commission National Institutes of Health (US) Most of the current knowledge on the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions annotated in the reference genome of Drosophila melanogaster, in 91 samples from 60 worldwide natural populations. We identified a set of 300 polymorphic TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Besides, we identified a set of 21 fixed TEs also likely to be adaptive. Indeed, we, and others, found evidence of selection for 84 of these reference TE insertions. The analysis of the genes located nearby these 84 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affects expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well. JG is funded by the European Commission (https://erc.europa.eu/) grant number H2020-ERC-2014-CoG-647900. DAP is funded by the National Institutes of Health (https://www.nih.gov/) grant numbers R01-GM089926 and R35-GM118165. 2020-04-14T10:17:13Z 2020-04-14T10:17:13Z 2019-02-19 2020-04-14T10:17:13Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1371/journal.pgen.1007900 e-issn: 1553-7404 issn: 1553-7390 PLoS Genetics 15(2): e1007900 (2019) http://hdl.handle.net/10261/207488 10.1371/journal.pgen.1007900 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/100000002 30753202 #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/647900 Publisher's version http://doi.org/10.1371/journal.pgen.1007900 Sí open Public Library of Science
institution IBE ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ibe-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IBE España
description Most of the current knowledge on the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions annotated in the reference genome of Drosophila melanogaster, in 91 samples from 60 worldwide natural populations. We identified a set of 300 polymorphic TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Besides, we identified a set of 21 fixed TEs also likely to be adaptive. Indeed, we, and others, found evidence of selection for 84 of these reference TE insertions. The analysis of the genes located nearby these 84 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affects expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well.
author2 European Commission
author_facet European Commission
Rech, Gabriel E.
Bogaerts-Márquez, María
Barrón, Maite G.
Merenciano, Miriam
Villanueva-Cañas, José Luis
Horváth, Vivien
Fiston-Lavier, Anna-Sophie
Luyten, Isabelle
Venkataram, Sandeep
Quesneville, Hadi
Petrov, Dmitri A.
González Pérez, Josefa
format artículo
author Rech, Gabriel E.
Bogaerts-Márquez, María
Barrón, Maite G.
Merenciano, Miriam
Villanueva-Cañas, José Luis
Horváth, Vivien
Fiston-Lavier, Anna-Sophie
Luyten, Isabelle
Venkataram, Sandeep
Quesneville, Hadi
Petrov, Dmitri A.
González Pérez, Josefa
spellingShingle Rech, Gabriel E.
Bogaerts-Márquez, María
Barrón, Maite G.
Merenciano, Miriam
Villanueva-Cañas, José Luis
Horváth, Vivien
Fiston-Lavier, Anna-Sophie
Luyten, Isabelle
Venkataram, Sandeep
Quesneville, Hadi
Petrov, Dmitri A.
González Pérez, Josefa
Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
author_sort Rech, Gabriel E.
title Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
title_short Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
title_full Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
title_fullStr Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
title_full_unstemmed Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
title_sort stress response, behavior, and development are shaped by transposable element-induced mutations in drosophila
publisher Public Library of Science
publishDate 2019-02-19
url http://hdl.handle.net/10261/207488
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/100000002
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