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Early social experience has life-long effects on baseline but not stress-induced cortisol levels in a cooperatively breeding fish
In cooperatively breeding cichlid fish, the early social environment has lifelong effects on the offspring's behaviour, life-history trajectories and brain gene expression. Here, we asked whether the presence or absence of parents and subordinate helpers during early life also shapes fluctuatin...
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Published in: | Hormones and behavior 2021-02, Vol.128, p.104910-104910, Article 104910 |
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creator | Antunes, Diogo F. Reyes-Contreras, Maria Glauser, Gaétan Taborsky, Barbara |
description | In cooperatively breeding cichlid fish, the early social environment has lifelong effects on the offspring's behaviour, life-history trajectories and brain gene expression. Here, we asked whether the presence or absence of parents and subordinate helpers during early life also shapes fluctuating levels of cortisol, the major stress hormone in the cichlid Neolamprologus pulcher. To non-invasively characterize baseline and stress-induced cortisol levels, we adapted the ‘static’ holding-water method often used to collect waterborne steroid hormones in aquatic organisms by including a flow-through system allowing for repeated sampling without handling of the experimental subjects. We used 8-year-old N. pulcher either raised with (+F) or without (−F) parents and helpers in early life. We found that N. pulcher have a peak of their circadian cortisol cycle in the early morning, and that they habituated to the experimental procedure after four days. Therefore, we sampled the experimental fish in the afternoon after four days of habituation. −F fish had significantly lower baseline cortisol levels, whereas stress-induced cortisol levels did not differ between treatments. Thus, we show that the early social environment has life-long effects on aspects of the physiological stress system of the Hypothalamic-Pituitary-Interrenal (HPI) axis. We discuss how these differences in physiological state may have contributed to the specialization in different social and life-history trajectories of this species.
•Early social experience can program neurophysiological systems for life.•We developed a dynamic holding-water method to non-invasively measure cortisol responses in small fish.•Early social deprivation induced a lifelong reduced cortisol baseline in a highly social cichlid.•The cortisol response to a stressor was not affected by early social experience.•Early socially deprived N. pulcher had higher opercular beat rates OBR response to stressor. |
doi_str_mv | 10.1016/j.yhbeh.2020.104910 |
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•Early social experience can program neurophysiological systems for life.•We developed a dynamic holding-water method to non-invasively measure cortisol responses in small fish.•Early social deprivation induced a lifelong reduced cortisol baseline in a highly social cichlid.•The cortisol response to a stressor was not affected by early social experience.•Early socially deprived N. pulcher had higher opercular beat rates OBR response to stressor.</description><identifier>ISSN: 0018-506X</identifier><identifier>EISSN: 1095-6867</identifier><identifier>DOI: 10.1016/j.yhbeh.2020.104910</identifier><identifier>PMID: 33309816</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Breeding ; Cichlids ; Circadian rhythm ; Cortisol ; Early social environment ; Habituation ; Holding-water method ; HPI axis ; Hydrocortisone ; Opercular beat rate ; Social Environment ; Stress response ; Stress, Physiological ; Waterborne hormone</subject><ispartof>Hormones and behavior, 2021-02, Vol.128, p.104910-104910, Article 104910</ispartof><rights>2020 Elsevier Inc.</rights><rights>Copyright © 2020 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c359t-b19d8bcfff1a4d7c47c6cedc9f12d84aa025d7ddec7662dd5f7e0b238cd97b2f3</citedby><cites>FETCH-LOGICAL-c359t-b19d8bcfff1a4d7c47c6cedc9f12d84aa025d7ddec7662dd5f7e0b238cd97b2f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33309816$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Antunes, Diogo F.</creatorcontrib><creatorcontrib>Reyes-Contreras, Maria</creatorcontrib><creatorcontrib>Glauser, Gaétan</creatorcontrib><creatorcontrib>Taborsky, Barbara</creatorcontrib><title>Early social experience has life-long effects on baseline but not stress-induced cortisol levels in a cooperatively breeding fish</title><title>Hormones and behavior</title><addtitle>Horm Behav</addtitle><description>In cooperatively breeding cichlid fish, the early social environment has lifelong effects on the offspring's behaviour, life-history trajectories and brain gene expression. Here, we asked whether the presence or absence of parents and subordinate helpers during early life also shapes fluctuating levels of cortisol, the major stress hormone in the cichlid Neolamprologus pulcher. To non-invasively characterize baseline and stress-induced cortisol levels, we adapted the ‘static’ holding-water method often used to collect waterborne steroid hormones in aquatic organisms by including a flow-through system allowing for repeated sampling without handling of the experimental subjects. We used 8-year-old N. pulcher either raised with (+F) or without (−F) parents and helpers in early life. We found that N. pulcher have a peak of their circadian cortisol cycle in the early morning, and that they habituated to the experimental procedure after four days. Therefore, we sampled the experimental fish in the afternoon after four days of habituation. −F fish had significantly lower baseline cortisol levels, whereas stress-induced cortisol levels did not differ between treatments. Thus, we show that the early social environment has life-long effects on aspects of the physiological stress system of the Hypothalamic-Pituitary-Interrenal (HPI) axis. We discuss how these differences in physiological state may have contributed to the specialization in different social and life-history trajectories of this species.
•Early social experience can program neurophysiological systems for life.•We developed a dynamic holding-water method to non-invasively measure cortisol responses in small fish.•Early social deprivation induced a lifelong reduced cortisol baseline in a highly social cichlid.•The cortisol response to a stressor was not affected by early social experience.•Early socially deprived N. pulcher had higher opercular beat rates OBR response to stressor.</description><subject>Animals</subject><subject>Breeding</subject><subject>Cichlids</subject><subject>Circadian rhythm</subject><subject>Cortisol</subject><subject>Early social environment</subject><subject>Habituation</subject><subject>Holding-water method</subject><subject>HPI axis</subject><subject>Hydrocortisone</subject><subject>Opercular beat rate</subject><subject>Social Environment</subject><subject>Stress response</subject><subject>Stress, Physiological</subject><subject>Waterborne hormone</subject><issn>0018-506X</issn><issn>1095-6867</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kMlKZDEUhoO0aDk8gdBk2ZtbJrnzwkUjTiC4UXAXMpxYKVI31Tn3irX0zU1Z2ktXh_PzD_ARcsbZnDPenC_nm4WGxVwwsVWqnrM9MuOsr4uma9pfZMYY74qaNc-H5AhxmV9eV9UBOSzLkvUdb2bk_UqlsKEYjVeBwtsakofBAF0opME7KEIcXig4B2ZEGgeqFULwA1A9jXSII8UxAWLhBzsZsNTENHqMgQZ4hYDUD1RlMeZmNfosbahOANbnWudxcUL2nQoIp1_3mDxdXz1e3hb3Dzd3l3_vC1PW_Vho3ttOG-ccV5VtTdWaJs-Z3nFhu0opJmrbWgumbRphbe1aYFqUnbF9q4Urj8mfXe86xX8T4ChXHg2EoAaIE0pRtSx3sEpka7mzmhQREzi5Tn6l0kZyJrfs5VJ-spdb9nLHPqd-fw1MegX2f-YbdjZc7AwZC7x6SBLNJ2zrU6YrbfQ_DnwAMLWZ8Q</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Antunes, Diogo F.</creator><creator>Reyes-Contreras, Maria</creator><creator>Glauser, Gaétan</creator><creator>Taborsky, Barbara</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>202102</creationdate><title>Early social experience has life-long effects on baseline but not stress-induced cortisol levels in a cooperatively breeding fish</title><author>Antunes, Diogo F. ; Reyes-Contreras, Maria ; Glauser, Gaétan ; Taborsky, Barbara</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c359t-b19d8bcfff1a4d7c47c6cedc9f12d84aa025d7ddec7662dd5f7e0b238cd97b2f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Breeding</topic><topic>Cichlids</topic><topic>Circadian rhythm</topic><topic>Cortisol</topic><topic>Early social environment</topic><topic>Habituation</topic><topic>Holding-water method</topic><topic>HPI axis</topic><topic>Hydrocortisone</topic><topic>Opercular beat rate</topic><topic>Social Environment</topic><topic>Stress response</topic><topic>Stress, Physiological</topic><topic>Waterborne hormone</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Antunes, Diogo F.</creatorcontrib><creatorcontrib>Reyes-Contreras, Maria</creatorcontrib><creatorcontrib>Glauser, Gaétan</creatorcontrib><creatorcontrib>Taborsky, Barbara</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Hormones and behavior</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Antunes, Diogo F.</au><au>Reyes-Contreras, Maria</au><au>Glauser, Gaétan</au><au>Taborsky, Barbara</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Early social experience has life-long effects on baseline but not stress-induced cortisol levels in a cooperatively breeding fish</atitle><jtitle>Hormones and behavior</jtitle><addtitle>Horm Behav</addtitle><date>2021-02</date><risdate>2021</risdate><volume>128</volume><spage>104910</spage><epage>104910</epage><pages>104910-104910</pages><artnum>104910</artnum><issn>0018-506X</issn><eissn>1095-6867</eissn><abstract>In cooperatively breeding cichlid fish, the early social environment has lifelong effects on the offspring's behaviour, life-history trajectories and brain gene expression. Here, we asked whether the presence or absence of parents and subordinate helpers during early life also shapes fluctuating levels of cortisol, the major stress hormone in the cichlid Neolamprologus pulcher. To non-invasively characterize baseline and stress-induced cortisol levels, we adapted the ‘static’ holding-water method often used to collect waterborne steroid hormones in aquatic organisms by including a flow-through system allowing for repeated sampling without handling of the experimental subjects. We used 8-year-old N. pulcher either raised with (+F) or without (−F) parents and helpers in early life. We found that N. pulcher have a peak of their circadian cortisol cycle in the early morning, and that they habituated to the experimental procedure after four days. Therefore, we sampled the experimental fish in the afternoon after four days of habituation. −F fish had significantly lower baseline cortisol levels, whereas stress-induced cortisol levels did not differ between treatments. Thus, we show that the early social environment has life-long effects on aspects of the physiological stress system of the Hypothalamic-Pituitary-Interrenal (HPI) axis. We discuss how these differences in physiological state may have contributed to the specialization in different social and life-history trajectories of this species.
•Early social experience can program neurophysiological systems for life.•We developed a dynamic holding-water method to non-invasively measure cortisol responses in small fish.•Early social deprivation induced a lifelong reduced cortisol baseline in a highly social cichlid.•The cortisol response to a stressor was not affected by early social experience.•Early socially deprived N. pulcher had higher opercular beat rates OBR response to stressor.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>33309816</pmid><doi>10.1016/j.yhbeh.2020.104910</doi><tpages>1</tpages></addata></record> |
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subjects | Animals Breeding Cichlids Circadian rhythm Cortisol Early social environment Habituation Holding-water method HPI axis Hydrocortisone Opercular beat rate Social Environment Stress response Stress, Physiological Waterborne hormone |
title | Early social experience has life-long effects on baseline but not stress-induced cortisol levels in a cooperatively breeding fish |
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