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Rank- and sex-specific differences in the neuroendocrine regulation of glucocorticoids in a wild group-living fish
Individuals that live in groups experience different challenges based on their social rank and sex. Glucocorticoids have a well-established role in coordinating responses to challenges and glucocorticoid levels often vary between ranks and sexes. However, the neuroendocrine mechanisms regulating glu...
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Published in: | Hormones and behavior 2021-11, Vol.136, p.105079-105079, Article 105079 |
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description | Individuals that live in groups experience different challenges based on their social rank and sex. Glucocorticoids have a well-established role in coordinating responses to challenges and glucocorticoid levels often vary between ranks and sexes. However, the neuroendocrine mechanisms regulating glucocorticoid dynamics in wild groups are poorly understood, making it difficult to determine the functional consequences of differences in glucocorticoid levels. Therefore, we observed wild social groups of a cooperatively breeding fish (Neolamprologus pulcher) and evaluated how scale cortisol content (an emerging method to evaluate cortisol dynamics in fishes) and expression of glucocorticoid-related genes varied across group members. Scale cortisol was detectable in ~50% of dominant males (7/17) and females (7/15)—but not in any subordinates (0/16)—suggesting that glucocorticoid levels were higher in dominants. However, the apparent behavioural and neuroendocrine factors regulating cortisol levels varied between dominant sexes. In dominant females, higher cortisol was associated with greater rates of territory defense and increased expression of corticotropin-releasing factor in the preoptic and hypothalamic regions of the brain, but these patterns were not observed in dominant males. Additionally, transcriptional differences in the liver suggest that dominant sexes may use different mechanisms to cope with elevated cortisol levels. While dominant females appeared to reduce the relative sensitivity of their liver to cortisol (fewer corticosteroid receptor transcripts), dominant males appeared to increase hepatic cortisol breakdown (more catabolic enzyme transcripts). Overall, our results offer valuable insights on the mechanisms regulating rank- and sex-based glucocorticoid dynamics, as well as the potential functional outcomes of these differences.
•We investigated how glucocorticoids are regulated in a wild group-living fish.•Scale cortisol content was only detectable in dominant fish and not subordinate fish.•Dominant females with higher cortisol were more aggressive and had higher CRF levels.•Dominant sexes used distinct strategies to reduce cortisol's actions on the liver.•Glucocorticoids are regulated differently across social ranks and between sexes. |
doi_str_mv | 10.1016/j.yhbeh.2021.105079 |
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•We investigated how glucocorticoids are regulated in a wild group-living fish.•Scale cortisol content was only detectable in dominant fish and not subordinate fish.•Dominant females with higher cortisol were more aggressive and had higher CRF levels.•Dominant sexes used distinct strategies to reduce cortisol's actions on the liver.•Glucocorticoids are regulated differently across social ranks and between sexes.</description><identifier>ISSN: 0018-506X</identifier><identifier>EISSN: 1095-6867</identifier><identifier>DOI: 10.1016/j.yhbeh.2021.105079</identifier><identifier>PMID: 34717080</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>11β-Hydroxysteroid dehydrogenase type 2 ; Animals ; Cichlids - physiology ; Corticotropin-releasing factor ; Corticotropin-Releasing Hormone - genetics ; Cortisol ; Female ; Glucocorticoid receptors ; Glucocorticoids - metabolism ; Hydrocortisone ; Male ; Neolamprologus pulcher ; Sex Characteristics ; Stress</subject><ispartof>Hormones and behavior, 2021-11, Vol.136, p.105079-105079, Article 105079</ispartof><rights>2021 The Authors</rights><rights>Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c404t-a05c93054d65ef9c8147aa80ca68ed1bfc651d37da965a308b76e8e373ce5eab3</citedby><cites>FETCH-LOGICAL-c404t-a05c93054d65ef9c8147aa80ca68ed1bfc651d37da965a308b76e8e373ce5eab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34717080$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Culbert, Brett M.</creatorcontrib><creatorcontrib>Ligocki, Isaac Y.</creatorcontrib><creatorcontrib>Salena, Matthew G.</creatorcontrib><creatorcontrib>Wong, Marian Y.L.</creatorcontrib><creatorcontrib>Hamilton, Ian M.</creatorcontrib><creatorcontrib>Aubin-Horth, Nadia</creatorcontrib><creatorcontrib>Bernier, Nicholas J.</creatorcontrib><creatorcontrib>Balshine, Sigal</creatorcontrib><title>Rank- and sex-specific differences in the neuroendocrine regulation of glucocorticoids in a wild group-living fish</title><title>Hormones and behavior</title><addtitle>Horm Behav</addtitle><description>Individuals that live in groups experience different challenges based on their social rank and sex. Glucocorticoids have a well-established role in coordinating responses to challenges and glucocorticoid levels often vary between ranks and sexes. However, the neuroendocrine mechanisms regulating glucocorticoid dynamics in wild groups are poorly understood, making it difficult to determine the functional consequences of differences in glucocorticoid levels. Therefore, we observed wild social groups of a cooperatively breeding fish (Neolamprologus pulcher) and evaluated how scale cortisol content (an emerging method to evaluate cortisol dynamics in fishes) and expression of glucocorticoid-related genes varied across group members. Scale cortisol was detectable in ~50% of dominant males (7/17) and females (7/15)—but not in any subordinates (0/16)—suggesting that glucocorticoid levels were higher in dominants. However, the apparent behavioural and neuroendocrine factors regulating cortisol levels varied between dominant sexes. In dominant females, higher cortisol was associated with greater rates of territory defense and increased expression of corticotropin-releasing factor in the preoptic and hypothalamic regions of the brain, but these patterns were not observed in dominant males. Additionally, transcriptional differences in the liver suggest that dominant sexes may use different mechanisms to cope with elevated cortisol levels. While dominant females appeared to reduce the relative sensitivity of their liver to cortisol (fewer corticosteroid receptor transcripts), dominant males appeared to increase hepatic cortisol breakdown (more catabolic enzyme transcripts). Overall, our results offer valuable insights on the mechanisms regulating rank- and sex-based glucocorticoid dynamics, as well as the potential functional outcomes of these differences.
•We investigated how glucocorticoids are regulated in a wild group-living fish.•Scale cortisol content was only detectable in dominant fish and not subordinate fish.•Dominant females with higher cortisol were more aggressive and had higher CRF levels.•Dominant sexes used distinct strategies to reduce cortisol's actions on the liver.•Glucocorticoids are regulated differently across social ranks and between sexes.</description><subject>11β-Hydroxysteroid dehydrogenase type 2</subject><subject>Animals</subject><subject>Cichlids - physiology</subject><subject>Corticotropin-releasing factor</subject><subject>Corticotropin-Releasing Hormone - genetics</subject><subject>Cortisol</subject><subject>Female</subject><subject>Glucocorticoid receptors</subject><subject>Glucocorticoids - metabolism</subject><subject>Hydrocortisone</subject><subject>Male</subject><subject>Neolamprologus pulcher</subject><subject>Sex Characteristics</subject><subject>Stress</subject><issn>0018-506X</issn><issn>1095-6867</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kMFu1DAQhi1URJfCEyAhH3vJMt7EjnPooapaQKqEhEDiZjn2eHeWrL21k9K-Pdlu6ZHTaEbfP6P5GPsgYClAqE_b5eOmx81yBSsxTyS03Su2ENDJSmnVnrAFgNCVBPXrlL0tZTu3QjbNG3ZaN61oQcOC5e82_q64jZ4XfKjKHh0FctxTCJgxOiycIh83yCNOOWH0yWWKyDOup8GOlCJPga-HySWX8kgukX_KWP6HBs_XOU37aqB7imseqGzesdfBDgXfP9cz9vPm-sfVl-r22-evV5e3lWugGSsL0nU1yMYriaFzWjSttRqcVRq96INTUvi69bZT0tag-1ahxrqtHUq0fX3Gzo979zndTVhGs6PicBhsxDQVs5IdgFaykzNaH1GXUykZg9ln2tn8aASYg2yzNU-yzUG2OcqeUx-fD0z9Dv1L5p_dGbg4Aji_eU-YTXF0cOopoxuNT_TfA38B0yCTLw</recordid><startdate>202111</startdate><enddate>202111</enddate><creator>Culbert, Brett M.</creator><creator>Ligocki, Isaac Y.</creator><creator>Salena, Matthew G.</creator><creator>Wong, Marian Y.L.</creator><creator>Hamilton, Ian M.</creator><creator>Aubin-Horth, Nadia</creator><creator>Bernier, Nicholas J.</creator><creator>Balshine, Sigal</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><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>202111</creationdate><title>Rank- and sex-specific differences in the neuroendocrine regulation of glucocorticoids in a wild group-living fish</title><author>Culbert, Brett M. ; Ligocki, Isaac Y. ; Salena, Matthew G. ; Wong, Marian Y.L. ; Hamilton, Ian M. ; Aubin-Horth, Nadia ; Bernier, Nicholas J. ; Balshine, Sigal</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c404t-a05c93054d65ef9c8147aa80ca68ed1bfc651d37da965a308b76e8e373ce5eab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>11β-Hydroxysteroid dehydrogenase type 2</topic><topic>Animals</topic><topic>Cichlids - physiology</topic><topic>Corticotropin-releasing factor</topic><topic>Corticotropin-Releasing Hormone - genetics</topic><topic>Cortisol</topic><topic>Female</topic><topic>Glucocorticoid receptors</topic><topic>Glucocorticoids - metabolism</topic><topic>Hydrocortisone</topic><topic>Male</topic><topic>Neolamprologus pulcher</topic><topic>Sex Characteristics</topic><topic>Stress</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Culbert, Brett M.</creatorcontrib><creatorcontrib>Ligocki, Isaac Y.</creatorcontrib><creatorcontrib>Salena, Matthew G.</creatorcontrib><creatorcontrib>Wong, Marian Y.L.</creatorcontrib><creatorcontrib>Hamilton, Ian M.</creatorcontrib><creatorcontrib>Aubin-Horth, Nadia</creatorcontrib><creatorcontrib>Bernier, Nicholas J.</creatorcontrib><creatorcontrib>Balshine, Sigal</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>Culbert, Brett M.</au><au>Ligocki, Isaac Y.</au><au>Salena, Matthew G.</au><au>Wong, Marian Y.L.</au><au>Hamilton, Ian M.</au><au>Aubin-Horth, Nadia</au><au>Bernier, Nicholas J.</au><au>Balshine, Sigal</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Rank- and sex-specific differences in the neuroendocrine regulation of glucocorticoids in a wild group-living fish</atitle><jtitle>Hormones and behavior</jtitle><addtitle>Horm Behav</addtitle><date>2021-11</date><risdate>2021</risdate><volume>136</volume><spage>105079</spage><epage>105079</epage><pages>105079-105079</pages><artnum>105079</artnum><issn>0018-506X</issn><eissn>1095-6867</eissn><abstract>Individuals that live in groups experience different challenges based on their social rank and sex. Glucocorticoids have a well-established role in coordinating responses to challenges and glucocorticoid levels often vary between ranks and sexes. However, the neuroendocrine mechanisms regulating glucocorticoid dynamics in wild groups are poorly understood, making it difficult to determine the functional consequences of differences in glucocorticoid levels. Therefore, we observed wild social groups of a cooperatively breeding fish (Neolamprologus pulcher) and evaluated how scale cortisol content (an emerging method to evaluate cortisol dynamics in fishes) and expression of glucocorticoid-related genes varied across group members. Scale cortisol was detectable in ~50% of dominant males (7/17) and females (7/15)—but not in any subordinates (0/16)—suggesting that glucocorticoid levels were higher in dominants. However, the apparent behavioural and neuroendocrine factors regulating cortisol levels varied between dominant sexes. In dominant females, higher cortisol was associated with greater rates of territory defense and increased expression of corticotropin-releasing factor in the preoptic and hypothalamic regions of the brain, but these patterns were not observed in dominant males. Additionally, transcriptional differences in the liver suggest that dominant sexes may use different mechanisms to cope with elevated cortisol levels. While dominant females appeared to reduce the relative sensitivity of their liver to cortisol (fewer corticosteroid receptor transcripts), dominant males appeared to increase hepatic cortisol breakdown (more catabolic enzyme transcripts). Overall, our results offer valuable insights on the mechanisms regulating rank- and sex-based glucocorticoid dynamics, as well as the potential functional outcomes of these differences.
•We investigated how glucocorticoids are regulated in a wild group-living fish.•Scale cortisol content was only detectable in dominant fish and not subordinate fish.•Dominant females with higher cortisol were more aggressive and had higher CRF levels.•Dominant sexes used distinct strategies to reduce cortisol's actions on the liver.•Glucocorticoids are regulated differently across social ranks and between sexes.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34717080</pmid><doi>10.1016/j.yhbeh.2021.105079</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 11β-Hydroxysteroid dehydrogenase type 2 Animals Cichlids - physiology Corticotropin-releasing factor Corticotropin-Releasing Hormone - genetics Cortisol Female Glucocorticoid receptors Glucocorticoids - metabolism Hydrocortisone Male Neolamprologus pulcher Sex Characteristics Stress |
title | Rank- and sex-specific differences in the neuroendocrine regulation of glucocorticoids in a wild group-living fish |
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