Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution

Autores
Kittelmann, Sebastian; Buffry, Alexandra D.; Franke, Franziska A.; Almudi, Isabel; Yoth, Marianne; Sabarís Di Lorenzo, Gonzalo Julián; Couso, Juan Pablo; Nunes, Maria D. S.; Frankel, Nicolás; Gómez-Skarmeta, José Luis; Pueyo-Marques, Jose; Arif, Saad; McGregor, Alistair P.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary ?hotspots? are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the ?naked valley? on T2 femurs in Drosophila melanogaster is caused by reduced microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution.
Fil: Kittelmann, Sebastian. Oxford Brookes University; Reino Unido
Fil: Buffry, Alexandra D.. Oxford Brookes University; Reino Unido
Fil: Franke, Franziska A.. Oxford Brookes University; Reino Unido
Fil: Almudi, Isabel. Universidad Pablo de Olavide; España
Fil: Yoth, Marianne. Oxford Brookes University; Reino Unido
Fil: Sabarís Di Lorenzo, Gonzalo Julián. 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: Couso, Juan Pablo. Universidad Pablo de Olavide; España
Fil: Nunes, Maria D. S.. Oxford Brookes University; Reino Unido
Fil: Frankel, Nicolás. 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: Gómez-Skarmeta, José Luis. Universidad Pablo de Olavide; España
Fil: Pueyo-Marques, Jose. University of Sussex; Reino Unido
Fil: Arif, Saad. Oxford Brookes University; Reino Unido
Fil: McGregor, Alistair P.. Oxford Brookes University; Reino Unido
Materia
causas genéticas
diversidad orgánica
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:11336/85990
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/85990
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolutionKittelmann, SebastianBuffry, Alexandra D.Franke, Franziska A.Almudi, IsabelYoth, MarianneSabarís Di Lorenzo, Gonzalo JuliánCouso, Juan PabloNunes, Maria D. S.Frankel, NicolásGómez-Skarmeta, José LuisPueyo-Marques, JoseArif, SaadMcGregor, Alistair P.causas genéticasdiversidad orgánicahttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary ?hotspots? are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the ?naked valley? on T2 femurs in Drosophila melanogaster is caused by reduced microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution.Fil: Kittelmann, Sebastian. Oxford Brookes University; Reino UnidoFil: Buffry, Alexandra D.. Oxford Brookes University; Reino UnidoFil: Franke, Franziska A.. Oxford Brookes University; Reino UnidoFil: Almudi, Isabel. Universidad Pablo de Olavide; EspañaFil: Yoth, Marianne. Oxford Brookes University; Reino UnidoFil: Sabarís Di Lorenzo, Gonzalo Julián. 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: Couso, Juan Pablo. Universidad Pablo de Olavide; EspañaFil: Nunes, Maria D. S.. Oxford Brookes University; Reino UnidoFil: Frankel, Nicolás. 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: Gómez-Skarmeta, José Luis. Universidad Pablo de Olavide; EspañaFil: Pueyo-Marques, Jose. University of Sussex; Reino UnidoFil: Arif, Saad. Oxford Brookes University; Reino UnidoFil: McGregor, Alistair P.. Oxford Brookes University; Reino UnidoPublic Library of Science2018-05-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/85990Kittelmann, Sebastian; Buffry, Alexandra D.; Franke, Franziska A.; Almudi, Isabel; Yoth, Marianne; et al.; Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution; Public Library of Science; Plos Genetics; 14; 5; 3-5-2018; 1-211553-7390CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://dx.plos.org/10.1371/journal.pgen.1007375info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pgen.1007375info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:03:51Zoai:ri.conicet.gov.ar:11336/85990instacron: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:34982025-09-10 13:03:51.38CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
title Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
spellingShingle Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
Kittelmann, Sebastian
causas genéticas
diversidad orgánica
title_short Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
title_full Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
title_fullStr Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
title_full_unstemmed Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
title_sort Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution
dc.creator.none.fl_str_mv Kittelmann, Sebastian
Buffry, Alexandra D.
Franke, Franziska A.
Almudi, Isabel
Yoth, Marianne
Sabarís Di Lorenzo, Gonzalo Julián
Couso, Juan Pablo
Nunes, Maria D. S.
Frankel, Nicolás
Gómez-Skarmeta, José Luis
Pueyo-Marques, Jose
Arif, Saad
McGregor, Alistair P.
author Kittelmann, Sebastian
author_facet Kittelmann, Sebastian
Buffry, Alexandra D.
Franke, Franziska A.
Almudi, Isabel
Yoth, Marianne
Sabarís Di Lorenzo, Gonzalo Julián
Couso, Juan Pablo
Nunes, Maria D. S.
Frankel, Nicolás
Gómez-Skarmeta, José Luis
Pueyo-Marques, Jose
Arif, Saad
McGregor, Alistair P.
author_role author
author2 Buffry, Alexandra D.
Franke, Franziska A.
Almudi, Isabel
Yoth, Marianne
Sabarís Di Lorenzo, Gonzalo Julián
Couso, Juan Pablo
Nunes, Maria D. S.
Frankel, Nicolás
Gómez-Skarmeta, José Luis
Pueyo-Marques, Jose
Arif, Saad
McGregor, Alistair P.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv causas genéticas
diversidad orgánica
topic causas genéticas
diversidad orgánica
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary ?hotspots? are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the ?naked valley? on T2 femurs in Drosophila melanogaster is caused by reduced microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution.
Fil: Kittelmann, Sebastian. Oxford Brookes University; Reino Unido
Fil: Buffry, Alexandra D.. Oxford Brookes University; Reino Unido
Fil: Franke, Franziska A.. Oxford Brookes University; Reino Unido
Fil: Almudi, Isabel. Universidad Pablo de Olavide; España
Fil: Yoth, Marianne. Oxford Brookes University; Reino Unido
Fil: Sabarís Di Lorenzo, Gonzalo Julián. 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: Couso, Juan Pablo. Universidad Pablo de Olavide; España
Fil: Nunes, Maria D. S.. Oxford Brookes University; Reino Unido
Fil: Frankel, Nicolás. 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: Gómez-Skarmeta, José Luis. Universidad Pablo de Olavide; España
Fil: Pueyo-Marques, Jose. University of Sussex; Reino Unido
Fil: Arif, Saad. Oxford Brookes University; Reino Unido
Fil: McGregor, Alistair P.. Oxford Brookes University; Reino Unido
description Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary ?hotspots? are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the ?naked valley? on T2 femurs in Drosophila melanogaster is caused by reduced microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution.
publishDate 2018
dc.date.none.fl_str_mv 2018-05-03
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/11336/85990
Kittelmann, Sebastian; Buffry, Alexandra D.; Franke, Franziska A.; Almudi, Isabel; Yoth, Marianne; et al.; Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution; Public Library of Science; Plos Genetics; 14; 5; 3-5-2018; 1-21
1553-7390
CONICET Digital
CONICET
url http://hdl.handle.net/11336/85990
identifier_str_mv Kittelmann, Sebastian; Buffry, Alexandra D.; Franke, Franziska A.; Almudi, Isabel; Yoth, Marianne; et al.; Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution; Public Library of Science; Plos Genetics; 14; 5; 3-5-2018; 1-21
1553-7390
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://dx.plos.org/10.1371/journal.pgen.1007375
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pgen.1007375
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
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
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
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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score 12.993085

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