Publicação
Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain
| Resumo: | Group living animals must be able to express different behavior profiles depending on their social status. Therefore, the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. However, how social information is translated into a neurogenomic response and what are the specific cues in a social interaction that signal a change in social status are questions that have remained unanswered. Here, we show for the first time, to our knowledge, that the switch between status-specific neurogenomic states relies on the assessment of fight outcome rather than just on self- or opponent-only assessment of fighting ability. For this purpose, we manipulated the perception of fight outcome in male zebrafish and measured its impact on the brain transcriptome using a zebrafish whole genome gene chip. Males fought either a real opponent, and a winner and a loser were identified, or their own image on a mirror, in which case, despite expressing aggressive behavior, males did not experience either a victory or a defeat. Massive changes in the brain transcriptome were observed in real opponent fighters, with losers displaying both a higher number of differentially expressed genes and of coexpressed gene modules than winners. In contrast, mirror fighters expressed a neurogenomic state similar to that of noninteracting fish. The genes that responded to fight outcome included immediate early genes and genes involved in neuroplasticity and epigenetic modifications. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on mutual assessment of fighting ability. |
|---|---|
| Autores principais: | Oliveira, Rui Filipe |
| Outros Autores: | Simões, José Miguel; Teles, Magda; Oliveira, Catarina R.; Becker, Jorg D.; Lopes, João Sollari |
| Assunto: | Social dominance Mutual assessment Fighting Gene expression Social genomics |
| Ano: | 2016 |
| País: | Portugal |
| Tipo de documento: | artigo |
| Tipo de acesso: | acesso restrito |
| Instituição associada: | Ispa-Instituto Universitário |
| Idioma: | inglês |
| Origem: | Repositório do Ispa - Instituto Universitário |
| _version_ | 1868077194084876288 |
|---|---|
| author | Oliveira, Rui Filipe |
| author2 | Simões, José Miguel Teles, Magda Oliveira, Catarina R. Becker, Jorg D. Lopes, João Sollari |
| author2_role | author author author author author |
| author_facet | Oliveira, Rui Filipe Simões, José Miguel Teles, Magda Oliveira, Catarina R. Becker, Jorg D. Lopes, João Sollari |
| author_role | author |
| contributor_name_str_mv | Repositório do ISPA |
| country_str | PT |
| creators_json_txt | [{\"Person.name\":\"Oliveira, Rui Filipe\"},{\"Person.name\":\"Simões, José Miguel\"},{\"Person.name\":\"Teles, Magda\"},{\"Person.name\":\"Oliveira, Catarina R.\"},{\"Person.name\":\"Becker, Jorg D.\"},{\"Person.name\":\"Lopes, João Sollari\"}] |
| datacite.contributors.contributor.contributorName.fl_str_mv | Repositório do ISPA |
| datacite.creators.creator.creatorName.fl_str_mv | Oliveira, Rui Filipe Simões, José Miguel Teles, Magda Oliveira, Catarina R. Becker, Jorg D. Lopes, João Sollari |
| datacite.date.Accepted.fl_str_mv | 2016-01-01T00:00:00Z |
| datacite.date.available.fl_str_mv | 2016-04-06T14:03:22Z |
| datacite.date.embargoed.fl_str_mv | 2016-04-06T14:03:22Z |
| datacite.rights.fl_str_mv | http://purl.org/coar/access_right/c_16ec |
| datacite.subjects.subject.fl_str_mv | Social dominance Mutual assessment Fighting Gene expression Social genomics |
| datacite.titles.title.fl_str_mv | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| dc.contributor.none.fl_str_mv | Repositório do ISPA |
| dc.creator.none.fl_str_mv | Oliveira, Rui Filipe Simões, José Miguel Teles, Magda Oliveira, Catarina R. Becker, Jorg D. Lopes, João Sollari |
| dc.date.Accepted.fl_str_mv | 2016-01-01T00:00:00Z |
| dc.date.available.fl_str_mv | 2016-04-06T14:03:22Z |
| dc.date.embargoed.fl_str_mv | 2016-04-06T14:03:22Z |
| dc.format.none.fl_str_mv | application/pdf |
| dc.identifier.none.fl_str_mv | http://hdl.handle.net/10400.12/4518 |
| dc.language.none.fl_str_mv | eng |
| dc.publisher.none.fl_str_mv | National Academy of Science |
| dc.rights.none.fl_str_mv | http://purl.org/coar/access_right/c_16ec |
| dc.subject.none.fl_str_mv | Social dominance Mutual assessment Fighting Gene expression Social genomics |
| dc.title.fl_str_mv | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| dc.type.none.fl_str_mv | http://purl.org/coar/resource_type/c_6501 |
| description | Group living animals must be able to express different behavior profiles depending on their social status. Therefore, the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. However, how social information is translated into a neurogenomic response and what are the specific cues in a social interaction that signal a change in social status are questions that have remained unanswered. Here, we show for the first time, to our knowledge, that the switch between status-specific neurogenomic states relies on the assessment of fight outcome rather than just on self- or opponent-only assessment of fighting ability. For this purpose, we manipulated the perception of fight outcome in male zebrafish and measured its impact on the brain transcriptome using a zebrafish whole genome gene chip. Males fought either a real opponent, and a winner and a loser were identified, or their own image on a mirror, in which case, despite expressing aggressive behavior, males did not experience either a victory or a defeat. Massive changes in the brain transcriptome were observed in real opponent fighters, with losers displaying both a higher number of differentially expressed genes and of coexpressed gene modules than winners. In contrast, mirror fighters expressed a neurogenomic state similar to that of noninteracting fish. The genes that responded to fight outcome included immediate early genes and genes involved in neuroplasticity and epigenetic modifications. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on mutual assessment of fighting ability. |
| dirty | 0 |
| eu_rights_str_mv | restrictedAccess |
| format | article |
| fulltext.url.fl_str_mv | https://repositorio.ispa.pt/bitstreams/5edc0507-a6e3-4ed5-9057-a78f151e81b2/download |
| funding.funder.alternateName_str_mv | FCT |
| funding.funder.identifier_str_mv | http://doi.org/10.13039/501100001871 |
| funding.funder.name_str_mv | Fundação para a Ciência e a Tecnologia |
| funding.identifier_str_mv | EXCL/BIA-ANM/0549/2012 |
| 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 |
| id | ispa_79fc0f46cd4c794af5a08ea42d40de17 |
| identifier.url.fl_str_mv | http://hdl.handle.net/10400.12/4518 |
| instacron_str | ispa |
| 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:10400.12/4518 |
| organization_str_mv | urn:organizationAcronym:ispa |
| person_str_mv | Oliveira, Rui Filipe Simões, José Miguel Teles, Magda Oliveira, Catarina R. Becker, Jorg D. Lopes, João Sollari |
| publishDate | 2016 |
| publisher.none.fl_str_mv | National Academy of Science |
| reponame_str | Repositório do Ispa - Instituto Universitário |
| repository_id_str | urn:repositoryAcronym:ispa |
| service_str_mv | urn:repositoryAcronym:ispa |
| spelling | engNational Academy of Sciencept_PTGroup living animals must be able to express different behavior profiles depending on their social status. Therefore, the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. However, how social information is translated into a neurogenomic response and what are the specific cues in a social interaction that signal a change in social status are questions that have remained unanswered. Here, we show for the first time, to our knowledge, that the switch between status-specific neurogenomic states relies on the assessment of fight outcome rather than just on self- or opponent-only assessment of fighting ability. For this purpose, we manipulated the perception of fight outcome in male zebrafish and measured its impact on the brain transcriptome using a zebrafish whole genome gene chip. Males fought either a real opponent, and a winner and a loser were identified, or their own image on a mirror, in which case, despite expressing aggressive behavior, males did not experience either a victory or a defeat. Massive changes in the brain transcriptome were observed in real opponent fighters, with losers displaying both a higher number of differentially expressed genes and of coexpressed gene modules than winners. In contrast, mirror fighters expressed a neurogenomic state similar to that of noninteracting fish. The genes that responded to fight outcome included immediate early genes and genes involved in neuroplasticity and epigenetic modifications. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on mutual assessment of fighting ability.application/pdfpt_PTAssessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brainOliveira, Rui FilipeSimões, José MiguelTeles, MagdaOliveira, Catarina R.Becker, Jorg D.Lopes, João SollariHostingInstitutionOrganizationalRepositório do ISPAe-mailmailto:repositorio@ispa.ptrepositorio@ispa.ptISSNIsPartOf0027-8424DOIIsPartOf10.1073/pnas.15142921132016-04-06T14:03:22Z20162016-01-01T00:00:00ZHandlehttp://hdl.handle.net/10400.12/4518http://purl.org/coar/access_right/c_16ecrestricted accessSocial dominanceMutual assessmentFightingGene expressionSocial genomics997547 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/10.13039/501100001871literaturehttp://purl.org/coar/resource_type/c_6501journal articlehttp://purl.org/coar/access_right/c_16ecapplication/pdffulltexthttps://repositorio.ispa.pt/bitstreams/5edc0507-a6e3-4ed5-9057-a78f151e81b2/downloadProceedings of the National Academy of Sciences11318 |
| spellingShingle | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain Oliveira, Rui Filipe Social dominance Mutual assessment Fighting Gene expression Social genomics |
| status | SINGLETON |
| subject.fl_str_mv | Social dominance Mutual assessment Fighting Gene expression Social genomics |
| title | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| title_full | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| title_fullStr | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| title_full_unstemmed | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| title_short | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| title_sort | Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain |
| topic | Social dominance Mutual assessment Fighting Gene expression Social genomics |
| topic_facet | Social dominance Mutual assessment Fighting Gene expression Social genomics |
| url | http://hdl.handle.net/10400.12/4518 |
| visible | 1 |
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