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Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish

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Resumo:Distinct patterns of gene expression often underlie intra- and intersexual differences, and the study of this set of coregulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behaviour (i.e., females are the courting sex) and sequential alternative reproductive tactics in males (i.e., larger and older nest-holder males and smaller and younger sneaker males occur). Sneakers mimic both female's courtship behaviour and nuptial coloration to get access to nests and sneak fertilizations, and later in life transition into nest-holder males. Thus, this species offers the unique opportunity to study how the regulation of gene expression can contribute to intersex phenotypes and to the sequential expression of male and female behavioural phenotypes by the same individual. We found that at the whole brain level, expression of the sneaker tactic was paralleled by broader and divergent gene expression when compared to either females or nest-holder males, which were more similar between themselves. When looking at sex-biased transcripts, sneaker males are intersex rather than being either nest-holder or female-like, and their transcriptome is simultaneously demasculinized for nest-holder-biased transcripts and feminized for female-biased transcripts. These results indicate that evolutionary changes in reproductive plasticity can be achieved through regulation of gene expression, and in particular by varying the magnitude of expression of sex-biased genes, throughout the lifetime of the same individual.
Autores principais:Cardoso, Sara
Outros Autores:Gonçalves, David; Goesmann, Alexander; Canário, Adelino V. M.; Oliveira, Rui Filipe
Assunto:Alternative reproductive tactics Behavioural plasticity Neurogenomic state RNA-seq Salaria Pavo Sex-biased gene expression
Ano:2018
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso restrito
Instituição associada:Ispa-Instituto Universitário
Idioma:inglês
Origem:Repositório do Ispa - Instituto Universitário
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author Cardoso, Sara
author2 Gonçalves, David
Goesmann, Alexander
Canário, Adelino V. M.
Oliveira, Rui Filipe
author2_role author
author
author
author
author_facet Cardoso, Sara
Gonçalves, David
Goesmann, Alexander
Canário, Adelino V. M.
Oliveira, Rui Filipe
author_role author
contributor_name_str_mv Repositório do ISPA
country_str PT
creators_json_txt [{\"Person.name\":\"Cardoso, Sara\",\"Person.identifier.orcid\":\"0000-0002-1006-2323\"},{\"Person.name\":\"Gonçalves, David\"},{\"Person.name\":\"Goesmann, Alexander\",\"Person.identifier.orcid\":\"0000-0002-7086-2568\"},{\"Person.name\":\"Canário, Adelino V. M.\"},{\"Person.name\":\"Oliveira, Rui Filipe\"}]
datacite.contributors.contributor.contributorName.fl_str_mv Repositório do ISPA
datacite.creators.creator.creatorName.fl_str_mv Cardoso, Sara
Gonçalves, David
Goesmann, Alexander
Canário, Adelino V. M.
Oliveira, Rui Filipe
datacite.date.Accepted.fl_str_mv 2018-01-01T00:00:00Z
datacite.date.available.fl_str_mv 2019-04-08T17:38:07Z
datacite.date.embargoed.fl_str_mv 2019-04-08T17:38:07Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_16ec
datacite.subjects.subject.fl_str_mv Alternative reproductive tactics
Behavioural plasticity
Neurogenomic state
RNA-seq
Salaria Pavo
Sex-biased gene expression
datacite.titles.title.fl_str_mv Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
dc.contributor.none.fl_str_mv Repositório do ISPA
dc.creator.none.fl_str_mv Cardoso, Sara
Gonçalves, David
Goesmann, Alexander
Canário, Adelino V. M.
Oliveira, Rui Filipe
dc.date.Accepted.fl_str_mv 2018-01-01T00:00:00Z
dc.date.available.fl_str_mv 2019-04-08T17:38:07Z
dc.date.embargoed.fl_str_mv 2019-04-08T17:38:07Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10400.12/6986
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Blackwell Publishing Inc.
dc.rights.cclincense.fl_str_mv http://creativecommons.org/licenses/by-nc/4.0/
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_16ec
dc.subject.none.fl_str_mv Alternative reproductive tactics
Behavioural plasticity
Neurogenomic state
RNA-seq
Salaria Pavo
Sex-biased gene expression
dc.title.fl_str_mv Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description Distinct patterns of gene expression often underlie intra- and intersexual differences, and the study of this set of coregulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behaviour (i.e., females are the courting sex) and sequential alternative reproductive tactics in males (i.e., larger and older nest-holder males and smaller and younger sneaker males occur). Sneakers mimic both female's courtship behaviour and nuptial coloration to get access to nests and sneak fertilizations, and later in life transition into nest-holder males. Thus, this species offers the unique opportunity to study how the regulation of gene expression can contribute to intersex phenotypes and to the sequential expression of male and female behavioural phenotypes by the same individual. We found that at the whole brain level, expression of the sneaker tactic was paralleled by broader and divergent gene expression when compared to either females or nest-holder males, which were more similar between themselves. When looking at sex-biased transcripts, sneaker males are intersex rather than being either nest-holder or female-like, and their transcriptome is simultaneously demasculinized for nest-holder-biased transcripts and feminized for female-biased transcripts. These results indicate that evolutionary changes in reproductive plasticity can be achieved through regulation of gene expression, and in particular by varying the magnitude of expression of sex-biased genes, throughout the lifetime of the same individual.
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fulltext.url.fl_str_mv https://repositorio.ispa.pt/bitstreams/d64b53e5-5dc8-4a4b-a149-57da0e812d63/download
funding.funder.alternateName_str_mv FCT
FCT
funding.funder.identifier_str_mv http://doi.org/10.13039/501100001871
http://doi.org/10.13039/501100001871
funding.funder.name_str_mv Fundação para a Ciência e a Tecnologia
Fundação para a Ciência e a Tecnologia
funding.identifier_str_mv EXCL/BIA-ANM/0549/2012
SFRH/BD/89072/2012
funding.name_str_mv 3599-PPCDT
funding_str_mv EXCL/BIA-ANM/0549/2012
info:eu-repo/grantAgreement/FCT/3599-PPCDT/EXCL%2FBIA-ANM%2F0549%2F2012/PT
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identifier.url.fl_str_mv http://hdl.handle.net/10400.12/6986
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institution Ispa-Instituto Universitário
instname_str Ispa-Instituto Universitário
language eng
network_acronym_str ispa
network_name_str Repositório do Ispa - Instituto Universitário
oai_identifier_str oai:repositorio.ispa.pt:10400.12/6986
organization_str_mv urn:organizationAcronym:ispa
person_str_mv Cardoso, Sara
Cardoso, Sara
https://www.ciencia-id.pt/991E-446C-750C
991E-446C-750C
http://orcid.org/0000-0002-1006-2323
0000-0002-1006-2323
Gonçalves, David
Goesmann, Alexander
Goesmann, Alexander
http://orcid.org/0000-0002-7086-2568
0000-0002-7086-2568
Canário, Adelino V. M.
Oliveira, Rui Filipe
publishDate 2018
publisher.none.fl_str_mv Blackwell Publishing Inc.
reponame_str Repositório do Ispa - Instituto Universitário
repository_id_str urn:repositoryAcronym:ispa
service_str_mv urn:repositoryAcronym:ispa
spelling engBlackwell Publishing Inc.pt_PTDistinct patterns of gene expression often underlie intra- and intersexual differences, and the study of this set of coregulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behaviour (i.e., females are the courting sex) and sequential alternative reproductive tactics in males (i.e., larger and older nest-holder males and smaller and younger sneaker males occur). Sneakers mimic both female's courtship behaviour and nuptial coloration to get access to nests and sneak fertilizations, and later in life transition into nest-holder males. Thus, this species offers the unique opportunity to study how the regulation of gene expression can contribute to intersex phenotypes and to the sequential expression of male and female behavioural phenotypes by the same individual. We found that at the whole brain level, expression of the sneaker tactic was paralleled by broader and divergent gene expression when compared to either females or nest-holder males, which were more similar between themselves. When looking at sex-biased transcripts, sneaker males are intersex rather than being either nest-holder or female-like, and their transcriptome is simultaneously demasculinized for nest-holder-biased transcripts and feminized for female-biased transcripts. These results indicate that evolutionary changes in reproductive plasticity can be achieved through regulation of gene expression, and in particular by varying the magnitude of expression of sex-biased genes, throughout the lifetime of the same individual.application/pdfpt_PTTemporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fishPersonalCardoso, SaraDSpacehttp://dspace.org/items/00d0d929-5def-48bc-9b33-2b71381f2214DSpacehttp://dspace.org/items/00d0d929-5def-48bc-9b33-2b71381f2214CardosoSaraCiência IDhttps://www.ciencia-id.pt991E-446C-750CORCIDhttp://orcid.org0000-0002-1006-2323Researcher IDhttps://www.researcherid.comH-1372-2012Scopus Author IDhttps://www.scopus.com55889189700Scopus Author IDhttps://www.scopus.com58126196200Gonçalves, DavidPersonalGoesmann, AlexanderDSpacehttp://dspace.org/items/ad4f2c8f-9fe1-4f25-afa9-f97f8b710081DSpacehttp://dspace.org/items/ad4f2c8f-9fe1-4f25-afa9-f97f8b710081GoesmannAlexanderORCIDhttp://orcid.org0000-0002-7086-2568Canário, Adelino V. M.Oliveira, Rui FilipeHostingInstitutionOrganizationalRepositório do ISPAe-mailmailto:repositorio@ispa.ptrepositorio@ispa.ptISSNIsPartOf0962-1083DOIIsPartOf10.1111/mec.144082019-04-08T17:38:07Z20182018-01-01T00:00:00ZHandlehttp://hdl.handle.net/10400.12/6986http://purl.org/coar/access_right/c_16ecrestricted accessAlternative reproductive tacticsBehavioural plasticityNeurogenomic stateRNA-seqSalaria PavoSex-biased gene expression958276 bytesFundação para a Ciência e a TecnologiaMolecular mechanisms and evolutionary implications of social plasticityinfo:eu-repo/grantAgreement/FCT/3599-PPCDT/EXCL%2FBIA-ANM%2F0549%2F2012/PTEXCL/BIA-ANM/0549/20123599-PPCDTCrossref Funder IDhttp://doi.org/10.13039/501100001871Fundação para a Ciência e a TecnologiaRNA-SEQ APPLIED TO THE PEACOCK BLENNY SALARIA PAVO: UNVEILING THE GENE NETWORKS AND SIGNALLING PATHWAYS BEHIND PHENOTYPIC PLASTICITY IN A LITTORAL FISHinfo:eu-repo/grantAgreement/FCT//SFRH%2FBD%2F89072%2F2012/PTSFRH/BD/89072/2012Crossref Funder IDhttp://doi.org/10.13039/501100001871literaturehttp://purl.org/coar/resource_type/c_6501journal article2018http://creativecommons.org/licenses/by-nc/4.0/http://purl.org/coar/access_right/c_16ecapplication/pdffulltexthttps://repositorio.ispa.pt/bitstreams/d64b53e5-5dc8-4a4b-a149-57da0e812d63/downloadMolecular ecology273789803United Kingdom
spellingShingle Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
Cardoso, Sara
Alternative reproductive tactics
Behavioural plasticity
Neurogenomic state
RNA-seq
Salaria Pavo
Sex-biased gene expression
status SINGLETON
subject.fl_str_mv Alternative reproductive tactics
Behavioural plasticity
Neurogenomic state
RNA-seq
Salaria Pavo
Sex-biased gene expression
title Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
title_full Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
title_fullStr Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
title_full_unstemmed Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
title_short Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
title_sort Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish
topic Alternative reproductive tactics
Behavioural plasticity
Neurogenomic state
RNA-seq
Salaria Pavo
Sex-biased gene expression
topic_facet Alternative reproductive tactics
Behavioural plasticity
Neurogenomic state
RNA-seq
Salaria Pavo
Sex-biased gene expression
url http://hdl.handle.net/10400.12/6986
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