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 a...

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Main Authors: Gabriel E Rech, María Bogaerts-Márquez, Maite G Barrón, Miriam Merenciano, José Luis Villanueva-Cañas, Vivien Horváth, Anna-Sophie Fiston-Lavier, Isabelle Luyten, Sandeep Venkataram, Hadi Quesneville, Dmitri A Petrov, Josefa González
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-02-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1007900
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spelling doaj-f2545878ca9d4e739d0ba6a26eda839d2021-04-21T13:50:19ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-02-01152e100790010.1371/journal.pgen.1007900Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila.Gabriel E RechMaría Bogaerts-MárquezMaite G BarrónMiriam MerencianoJosé Luis Villanueva-CañasVivien HorváthAnna-Sophie Fiston-LavierIsabelle LuytenSandeep VenkataramHadi QuesnevilleDmitri A PetrovJosefa GonzálezMost 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.https://doi.org/10.1371/journal.pgen.1007900
collection DOAJ
language English
format Article
sources DOAJ
author Gabriel E Rech
María Bogaerts-Márquez
Maite G Barrón
Miriam Merenciano
José Luis Villanueva-Cañas
Vivien Horváth
Anna-Sophie Fiston-Lavier
Isabelle Luyten
Sandeep Venkataram
Hadi Quesneville
Dmitri A Petrov
Josefa González
spellingShingle Gabriel E Rech
María Bogaerts-Márquez
Maite G Barrón
Miriam Merenciano
José Luis Villanueva-Cañas
Vivien Horváth
Anna-Sophie Fiston-Lavier
Isabelle Luyten
Sandeep Venkataram
Hadi Quesneville
Dmitri A Petrov
Josefa González
Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila.
PLoS Genetics
author_facet Gabriel E Rech
María Bogaerts-Márquez
Maite G Barrón
Miriam Merenciano
José Luis Villanueva-Cañas
Vivien Horváth
Anna-Sophie Fiston-Lavier
Isabelle Luyten
Sandeep Venkataram
Hadi Quesneville
Dmitri A Petrov
Josefa González
author_sort Gabriel E Rech
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 (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2019-02-01
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.
url https://doi.org/10.1371/journal.pgen.1007900
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