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

Autores
Mensch, J.; Lavagnino, N.; Carreira, V.P.; Massaldi, A.; Hasson, E.; Fanara, J.J.
Año de publicación
2008
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fuente
BMC Dev. Biol. 2008;8
Materia
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
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by/2.5/ar
Repositorio
Biblioteca Digital (UBA-FCEN)
Institución
Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
OAI Identificador
paperaa:paper_1471213X_v8_n_p_Mensch

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oai_identifier_str paperaa:paper_1471213X_v8_n_p_Mensch
network_acronym_str BDUBAFCEN
repository_id_str 1896
network_name_str Biblioteca Digital (UBA-FCEN)
spelling Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interactionMensch, J.Lavagnino, N.Carreira, V.P.Massaldi, A.Hasson, E.Fanara, J.J.articledevelopmentDrosophila melanogastergenegene identificationgene insertiongene interactiongenetic traitgenetic variabilitygenotype phenotype correlationkarl genemerlin genemutantnonhumanpleiotropyanalysis of varianceanimaldevelopmental geneenvironmentfemalegenegene expression regulationgeneticsgrowth, development and agingmalephenotypetemperaturetimeDrosophila melanogasterHexapodaDrosophila proteinmerlinmerlin, DrosophilaAnalysis of VarianceAnimalsDrosophila melanogasterDrosophila ProteinsEnvironmentFemaleGene Expression Regulation, DevelopmentalGenes, DevelopmentalGenes, InsectMaleMutagenesis, InsertionalNeurofibromin 2PhenotypeTemperatureTime FactorsBackground. 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.2008info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12110/paper_1471213X_v8_n_p_MenschBMC Dev. Biol. 2008;8reponame:Biblioteca Digital (UBA-FCEN)instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesinstacron:UBA-FCENenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/2.5/ar2025-09-29T13:43:06Zpaperaa:paper_1471213X_v8_n_p_MenschInstitucionalhttps://digital.bl.fcen.uba.ar/Universidad públicaNo correspondehttps://digital.bl.fcen.uba.ar/cgi-bin/oaiserver.cgiana@bl.fcen.uba.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:18962025-09-29 13:43:07.306Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesfalse
dc.title.none.fl_str_mv Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
title Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
spellingShingle Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction
Mensch, 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
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
dc.creator.none.fl_str_mv Mensch, J.
Lavagnino, N.
Carreira, V.P.
Massaldi, A.
Hasson, E.
Fanara, J.J.
author Mensch, J.
author_facet Mensch, J.
Lavagnino, N.
Carreira, V.P.
Massaldi, A.
Hasson, E.
Fanara, J.J.
author_role author
author2 Lavagnino, N.
Carreira, V.P.
Massaldi, A.
Hasson, E.
Fanara, J.J.
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv 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
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
dc.description.none.fl_txt_mv 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.
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.
publishDate 2008
dc.date.none.fl_str_mv 2008
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12110/paper_1471213X_v8_n_p_Mensch
url http://hdl.handle.net/20.500.12110/paper_1471213X_v8_n_p_Mensch
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by/2.5/ar
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/2.5/ar
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv BMC Dev. Biol. 2008;8
reponame:Biblioteca Digital (UBA-FCEN)
instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron:UBA-FCEN
reponame_str Biblioteca Digital (UBA-FCEN)
collection Biblioteca Digital (UBA-FCEN)
instname_str Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron_str UBA-FCEN
institution UBA-FCEN
repository.name.fl_str_mv Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
repository.mail.fl_str_mv ana@bl.fcen.uba.ar
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