Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction

Background. Understanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometab...

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Autores principales: Mensch, J., Lavagnino, N., Carreira, V.P., Massaldi, A., Hasson, E., Fanara, J.J.
Formato: Artículo publishedVersion
Lenguaje:Inglés
Publicado: 2008
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_1471213X_v8_n_p_Mensch
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spelling paperaa:paper_1471213X_v8_n_p_Mensch2023-06-12T16:50:24Z Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction BMC Dev. Biol. 2008;8 Mensch, J. Lavagnino, N. Carreira, V.P. Massaldi, A. Hasson, E. Fanara, J.J. article development Drosophila melanogaster gene gene identification gene insertion gene interaction genetic trait genetic variability genotype phenotype correlation karl gene merlin gene mutant nonhuman pleiotropy analysis of variance animal developmental gene environment female gene gene expression regulation genetics growth, development and aging male phenotype temperature time Drosophila melanogaster Hexapoda Drosophila protein merlin merlin, Drosophila Analysis of Variance Animals Drosophila melanogaster Drosophila Proteins Environment Female Gene Expression Regulation, Developmental Genes, Developmental Genes, Insect Male Mutagenesis, Insertional Neurofibromin 2 Phenotype Temperature Time Factors Background. Understanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometabolous insects that occupy ephemeral habitats, like fruit flies, the impact of developmental time on fitness is further exaggerated. The present work is one of the first systematic studies of the genetic basis of developmental time, in which we also evaluate the impact of environmental variation on the expression of the trait. Results. We analyzed 179 co-isogenic single P[GT1]-element insertion lines of Drosophila melanogaster to identify novel genes affecting developmental time in flies reared at 25°C. Sixty percent of the lines showed a heterochronic phenotype, suggesting that a large number of genes affect this trait. Mutant lines for the genes Merlin and Karl showed the most extreme phenotypes exhibiting a developmental time reduction and increase, respectively, of over 2 days and 4 days relative to the control (a co-isogenic P-element insertion free line). In addition, a subset of 42 lines selected at random from the initial set of 179 lines was screened at 17°C. Interestingly, the gene-by-environment interaction accounted for 52% of total phenotypic variance. Plastic reaction norms were found for a large number of developmental time candidate genes. Conclusion. We identified components of several integrated time-dependent pathways affecting egg-to-adult developmental time in Drosophila. At the same time, we also show that many heterochronic phenotypes may arise from changes in genes involved in several developmental mechanisms that do not explicitly control the timing of specific events. We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development. Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait. © 2008 Mensch et al; licensee BioMed Central Ltd. Fil:Mensch, J. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Lavagnino, N. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Carreira, V.P. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Hasson, E. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Fanara, J.J. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. 2008 info:eu-repo/semantics/article info:ar-repo/semantics/artículo info:eu-repo/semantics/publishedVersion application/pdf eng info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_1471213X_v8_n_p_Mensch
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
language Inglés
orig_language_str_mv eng
topic article
development
Drosophila melanogaster
gene
gene identification
gene insertion
gene interaction
genetic trait
genetic variability
genotype phenotype correlation
karl gene
merlin gene
mutant
nonhuman
pleiotropy
analysis of variance
animal
developmental gene
environment
female
gene
gene expression regulation
genetics
growth, development and aging
male
phenotype
temperature
time
Drosophila melanogaster
Hexapoda
Drosophila protein
merlin
merlin, Drosophila
Analysis of Variance
Animals
Drosophila melanogaster
Drosophila Proteins
Environment
Female
Gene Expression Regulation, Developmental
Genes, Developmental
Genes, Insect
Male
Mutagenesis, Insertional
Neurofibromin 2
Phenotype
Temperature
Time Factors
spellingShingle article
development
Drosophila melanogaster
gene
gene identification
gene insertion
gene interaction
genetic trait
genetic variability
genotype phenotype correlation
karl gene
merlin gene
mutant
nonhuman
pleiotropy
analysis of variance
animal
developmental gene
environment
female
gene
gene expression regulation
genetics
growth, development and aging
male
phenotype
temperature
time
Drosophila melanogaster
Hexapoda
Drosophila protein
merlin
merlin, Drosophila
Analysis of Variance
Animals
Drosophila melanogaster
Drosophila Proteins
Environment
Female
Gene Expression Regulation, Developmental
Genes, Developmental
Genes, Insect
Male
Mutagenesis, Insertional
Neurofibromin 2
Phenotype
Temperature
Time Factors
Mensch, J.
Lavagnino, N.
Carreira, V.P.
Massaldi, A.
Hasson, E.
Fanara, J.J.
Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
topic_facet article
development
Drosophila melanogaster
gene
gene identification
gene insertion
gene interaction
genetic trait
genetic variability
genotype phenotype correlation
karl gene
merlin gene
mutant
nonhuman
pleiotropy
analysis of variance
animal
developmental gene
environment
female
gene
gene expression regulation
genetics
growth, development and aging
male
phenotype
temperature
time
Drosophila melanogaster
Hexapoda
Drosophila protein
merlin
merlin, Drosophila
Analysis of Variance
Animals
Drosophila melanogaster
Drosophila Proteins
Environment
Female
Gene Expression Regulation, Developmental
Genes, Developmental
Genes, Insect
Male
Mutagenesis, Insertional
Neurofibromin 2
Phenotype
Temperature
Time Factors
description Background. Understanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometabolous insects that occupy ephemeral habitats, like fruit flies, the impact of developmental time on fitness is further exaggerated. The present work is one of the first systematic studies of the genetic basis of developmental time, in which we also evaluate the impact of environmental variation on the expression of the trait. Results. We analyzed 179 co-isogenic single P[GT1]-element insertion lines of Drosophila melanogaster to identify novel genes affecting developmental time in flies reared at 25°C. Sixty percent of the lines showed a heterochronic phenotype, suggesting that a large number of genes affect this trait. Mutant lines for the genes Merlin and Karl showed the most extreme phenotypes exhibiting a developmental time reduction and increase, respectively, of over 2 days and 4 days relative to the control (a co-isogenic P-element insertion free line). In addition, a subset of 42 lines selected at random from the initial set of 179 lines was screened at 17°C. Interestingly, the gene-by-environment interaction accounted for 52% of total phenotypic variance. Plastic reaction norms were found for a large number of developmental time candidate genes. Conclusion. We identified components of several integrated time-dependent pathways affecting egg-to-adult developmental time in Drosophila. At the same time, we also show that many heterochronic phenotypes may arise from changes in genes involved in several developmental mechanisms that do not explicitly control the timing of specific events. We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development. Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait. © 2008 Mensch et al; licensee BioMed Central Ltd.
format Artículo
Artículo
publishedVersion
author Mensch, J.
Lavagnino, N.
Carreira, V.P.
Massaldi, A.
Hasson, E.
Fanara, J.J.
author_facet Mensch, J.
Lavagnino, N.
Carreira, V.P.
Massaldi, A.
Hasson, E.
Fanara, J.J.
author_sort Mensch, J.
title Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
title_short Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
title_full Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
title_fullStr Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
title_full_unstemmed Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
title_sort identifying candidate genes affecting developmental time in drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction
publishDate 2008
url http://hdl.handle.net/20.500.12110/paper_1471213X_v8_n_p_Mensch
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