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

Autor: Gabriel E. Rech, Anna-Sophie Fiston-Lavier, José Luis Villanueva-Cañas, Miriam Merenciano, Hadi Quesneville, Vivien Horváth, Sandeep Venkataram, Dmitri A. Petrov, Josefa González, Isabelle Luyten, Maite G. Barrón, Maria Bogaerts-Marquez
Přispěvatelé: European Commission, National Institutes of Health (US), Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS), National Institutes of Health [R01-GM089926, R35-GM118165], European Project: 647900,H2020,ERC-2014-CoG,DROSADAPTATION(2016), Unité de Recherche Génomique Info (URGI), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École pratique des hautes études (EPHE)
Rok vydání: 2019
Předmět:
0106 biological sciences
Chi square tests
Genome
Insect

population
adaptation
01 natural sciences
0302 clinical medicine
MESH: Animals
MESH: DNA Transposable Elements: genetics
0303 health sciences
education.field_of_study
Natural selection
Behavior
Animal

Organic Compounds
Statistics
Eukaryota
Genomics
Drosophila melanogaster
Physical Sciences
Gene ontologies
genetic-variation
Transposable element
MESH: Genome
Insect: genetics

sequence
evolution
melanogaster
reference panel
positive selection
insecticide resistance
genome-wide patterns
Single-nucleotide polymorphism
Evolution
Molecular

03 medical and health sciences
Invertebrate genomics
MESH: Mutation: genetics
MESH: Selection
Genetic: genetics

Genetics
Statistical Methods
education
Statistical Hypothesis Testing
Molecular Biology
Ecology
Evolution
Behavior and Systematics

[SDV.GEN]Life Sciences [q-bio]/Genetics
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
Organisms
Chemical Compounds
Biology and Life Sciences
Computational Biology
MESH: Gene Expression Regulation
Developmental: genetics

Invertebrates
Evolutionary biology
Mutation
Animal Studies
Gene expression
Adaptation
Mathematics
030217 neurology & neurosurgery
Cancer Research
MESH: Behavior
Animal: physiology

[SDV]Life Sciences [q-bio]
QH426-470
Evolutionary adaptation
Mathematical and Statistical Techniques
Gene Frequency
Genetics (clinical)
MESH: Evolution
Molecular

MESH: Gene Frequency: genetics
Gene Expression Regulation
Developmental

Animal Models
Phenotype
Insects
Chemistry
Experimental Organism Systems
MESH: Stress
Physiological: genetics

Drosophila
Research Article
Evolutionary Processes
Arthropoda
Population
MESH: Drosophila melanogaster: genetics
Biology
Research and Analysis Methods
Polymorphism
Single Nucleotide

010603 evolutionary biology
Model Organisms
Stress
Physiological

Genetic variation
Animals
Selection
Genetic

Gene
030304 developmental biology
Evolutionary Biology
Organic Chemistry
Genome analysis
biology.organism_classification
Animal Genomics
Alcohols
MESH: Polymorphism
Single Nucleotide: genetics

DNA Transposable Elements
Reference genome
Zdroj: PLoS Genetics
PLoS Genetics, 2019, 15 (2), pp.e1007900. ⟨10.1371/journal.pgen.1007900⟩
PLoS Genetics, Public Library of Science, 2019, 15 (2), pp.e1007900. ⟨10.1371/journal.pgen.1007900⟩
Digital.CSIC. Repositorio Institucional del CSIC
instname
PLOS Genetics
Recercat. Dipósit de la Recerca de Catalunya
PLoS Genetics, Vol 15, Iss 2, p e1007900 (2019)
Plos Genetics 2 (15), 1-33. (2019)
ISSN: 1553-7390
1553-7404
DOI: 10.1371/journal.pgen.1007900⟩
Popis: 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.
Author summary Transposable elements are fragments of genomic DNA that have the ability to move around the genome by creating new copies of themselves. Although there is evidence suggesting that transposable elements play important roles in genome function and genome evolution, our current understanding is based on the analysis of a subset of all transposable element insertions present in the genome, in only a few natural populations. Advances in genome sequencing and bioinformatics tools allow us now to investigate all transposable element insertions in genomes across continents. In this work, we analyzed the age, size, and frequency of 1,615 transposable elements in 91 samples from 60 worldwide natural populations of the model species Drosophila melanogaster. The genomic regions surrounding 84 transposable elements indicate that they could have an adaptive effect for the flies that carry them. These insertions are located nearby genes involved in stress response, behavior and development suggesting that these biological processes are affected by transposable element insertions.
Databáze: OpenAIRE