Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development

Autores
Mensch, Julian; Serra, François; Lavagnino, Nicolas Jose; Dopazo, Hernán Javier; Hasson, Esteban Ruben
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Developmental conservation among related species is a common generalization known as von Baer’s third law and implies that early stages of development are the most refractory to change. The “hourglass model” is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes,ourresults showed differential selective pressures atdifferentmoments ofembryogenesis. In manyDrosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. BecausemanyNupsareinvolvedinhybridincompatibilitiesbetweenspeciesoftheDrosophilamelanogastersubgroup,ourresultslink rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence.
Fil: Mensch, Julian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Serra, François. Centro de Investigaciones Principe Felipe; España. Centro Nacional de Análisis Genómico; España
Fil: Lavagnino, Nicolas Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Dopazo, Hernán Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Hasson, Esteban Ruben. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Materia
EMBRYONIC GENES
NUPS
HOURGLASS MODEL
DOSAGE COMPENSATION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/15851
Acceder
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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila developmentMensch, JulianSerra, FrançoisLavagnino, Nicolas JoseDopazo, Hernán JavierHasson, Esteban RubenEMBRYONIC GENESNUPSHOURGLASS MODELDOSAGE COMPENSATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Developmental conservation among related species is a common generalization known as von Baer’s third law and implies that early stages of development are the most refractory to change. The “hourglass model” is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes,ourresults showed differential selective pressures atdifferentmoments ofembryogenesis. In manyDrosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. BecausemanyNupsareinvolvedinhybridincompatibilitiesbetweenspeciesoftheDrosophilamelanogastersubgroup,ourresultslink rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence.Fil: Mensch, Julian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Serra, François. Centro de Investigaciones Principe Felipe; España. Centro Nacional de Análisis Genómico; EspañaFil: Lavagnino, Nicolas Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Dopazo, Hernán Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Hasson, Esteban Ruben. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaOxford University Press2013-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/15851Mensch, Julian; Serra, François; Lavagnino, Nicolas Jose; Dopazo, Hernán Javier; Hasson, Esteban Ruben; Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development; Oxford University Press; Genome Biology and Evolution; 5; 11; 10-2013; 2231-22411759-6653enginfo:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evt156info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/gbe/article-lookup/doi/10.1093/gbe/evt156info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3845637/info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:13:48Zoai:ri.conicet.gov.ar:11336/15851instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:13:48.467CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
title Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
spellingShingle Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
Mensch, Julian
EMBRYONIC GENES
NUPS
HOURGLASS MODEL
DOSAGE COMPENSATION
title_short Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
title_full Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
title_fullStr Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
title_full_unstemmed Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
title_sort Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development
dc.creator.none.fl_str_mv Mensch, Julian
Serra, François
Lavagnino, Nicolas Jose
Dopazo, Hernán Javier
Hasson, Esteban Ruben
author Mensch, Julian
author_facet Mensch, Julian
Serra, François
Lavagnino, Nicolas Jose
Dopazo, Hernán Javier
Hasson, Esteban Ruben
author_role author
author2 Serra, François
Lavagnino, Nicolas Jose
Dopazo, Hernán Javier
Hasson, Esteban Ruben
author2_role author
author
author
author
dc.subject.none.fl_str_mv EMBRYONIC GENES
NUPS
HOURGLASS MODEL
DOSAGE COMPENSATION
topic EMBRYONIC GENES
NUPS
HOURGLASS MODEL
DOSAGE COMPENSATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Developmental conservation among related species is a common generalization known as von Baer’s third law and implies that early stages of development are the most refractory to change. The “hourglass model” is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes,ourresults showed differential selective pressures atdifferentmoments ofembryogenesis. In manyDrosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. BecausemanyNupsareinvolvedinhybridincompatibilitiesbetweenspeciesoftheDrosophilamelanogastersubgroup,ourresultslink rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence.
Fil: Mensch, Julian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Serra, François. Centro de Investigaciones Principe Felipe; España. Centro Nacional de Análisis Genómico; España
Fil: Lavagnino, Nicolas Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Dopazo, Hernán Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Hasson, Esteban Ruben. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
description Developmental conservation among related species is a common generalization known as von Baer’s third law and implies that early stages of development are the most refractory to change. The “hourglass model” is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes,ourresults showed differential selective pressures atdifferentmoments ofembryogenesis. In manyDrosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. BecausemanyNupsareinvolvedinhybridincompatibilitiesbetweenspeciesoftheDrosophilamelanogastersubgroup,ourresultslink rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence.
publishDate 2013
dc.date.none.fl_str_mv 2013-10
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/11336/15851
Mensch, Julian; Serra, François; Lavagnino, Nicolas Jose; Dopazo, Hernán Javier; Hasson, Esteban Ruben; Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development; Oxford University Press; Genome Biology and Evolution; 5; 11; 10-2013; 2231-2241
1759-6653
url http://hdl.handle.net/11336/15851
identifier_str_mv Mensch, Julian; Serra, François; Lavagnino, Nicolas Jose; Dopazo, Hernán Javier; Hasson, Esteban Ruben; Positive selection in Nucleoporins challenges constraints on early expressed genes in Drosophila development; Oxford University Press; Genome Biology and Evolution; 5; 11; 10-2013; 2231-2241
1759-6653
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evt156
info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/gbe/article-lookup/doi/10.1093/gbe/evt156
info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3845637/
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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