Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses
Fishes exhibit remarkably diverse, and plastic, patterns of sexual development, most striking of which is sequential hermaphroditism, where individuals readily reverse sex in adulthood. How this stunning example of phenotypic plasticity is controlled at a genetic level remains poorly understood. Sev...
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| Format: | Article |
| Language: | English |
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PeerJ Inc.
2019-06-01
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| Series: | PeerJ |
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| Online Access: | https://peerj.com/articles/7032.pdf |
| _version_ | 1797420195325673472 |
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| author | Jodi T. Thomas Erica V. Todd Simon Muncaster P Mark Lokman Erin L. Damsteegt Hui Liu Kiyoshi Soyano Florence Gléonnec Melissa S. Lamm John R. Godwin Neil J. Gemmell |
| author_facet | Jodi T. Thomas Erica V. Todd Simon Muncaster P Mark Lokman Erin L. Damsteegt Hui Liu Kiyoshi Soyano Florence Gléonnec Melissa S. Lamm John R. Godwin Neil J. Gemmell |
| author_sort | Jodi T. Thomas |
| collection | DOAJ |
| description | Fishes exhibit remarkably diverse, and plastic, patterns of sexual development, most striking of which is sequential hermaphroditism, where individuals readily reverse sex in adulthood. How this stunning example of phenotypic plasticity is controlled at a genetic level remains poorly understood. Several genes have been implicated in regulating sex change, yet the degree to which a conserved genetic machinery orchestrates this process has not yet been addressed. Using captive and in-the-field social manipulations to initiate sex change, combined with a comparative qPCR approach, we compared expression patterns of four candidate regulatory genes among three species of wrasses (Labridae)—a large and diverse teleost family where female-to-male sex change is pervasive, socially-cued, and likely ancestral. Expression in brain and gonadal tissues were compared among the iconic tropical bluehead wrasse (Thalassoma bifasciatum) and the temperate spotty (Notolabrus celidotus) and kyusen (Parajulus poecilepterus) wrasses. In all three species, gonadal sex change was preceded by downregulation of cyp19a1a (encoding gonadal aromatase that converts androgens to oestrogens) and accompanied by upregulation of amh (encoding anti-müllerian hormone that primarily regulates male germ cell development), and these genes may act concurrently to orchestrate ovary-testis transformation. In the brain, our data argue against a role for brain aromatase (cyp19a1b) in initiating behavioural sex change, as its expression trailed behavioural changes. However, we find that isotocin (it, that regulates teleost socio-sexual behaviours) expression correlated with dominant male-specific behaviours in the bluehead wrasse, suggesting it upregulation mediates the rapid behavioural sex change characteristic of blueheads and other tropical wrasses. However, it expression was not sex-biased in temperate spotty and kyusen wrasses, where sex change is more protracted and social groups may be less tightly-structured. Together, these findings suggest that while key components of the molecular machinery controlling gonadal sex change are phylogenetically conserved among wrasses, neural pathways governing behavioural sex change may be more variable. |
| first_indexed | 2024-03-09T06:58:10Z |
| format | Article |
| id | doaj.art-71803159887b473881613e5cf09eef5f |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T06:58:10Z |
| publishDate | 2019-06-01 |
| publisher | PeerJ Inc. |
| record_format | Article |
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| spelling | doaj.art-71803159887b473881613e5cf09eef5f2023-12-03T09:59:26ZengPeerJ Inc.PeerJ2167-83592019-06-017e703210.7717/peerj.7032Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrassesJodi T. Thomas0Erica V. Todd1Simon Muncaster2P Mark Lokman3Erin L. Damsteegt4Hui Liu5Kiyoshi Soyano6Florence Gléonnec7Melissa S. Lamm8John R. Godwin9Neil J. Gemmell10ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, AustraliaDepartment of Anatomy, University of Otago, Dunedin, Otago, New ZealandFaculty of Primary Industries, Environment and Science, Toi Ohomai Institute of Technology, Tauranga, Bay of Plenty, New ZealandDepartment of Zoology, University of Otago, Dunedin, Otago, New ZealandDepartment of Zoology, University of Otago, Dunedin, Otago, New ZealandDepartment of Anatomy, University of Otago, Dunedin, Otago, New ZealandInstitute for East China Sea Research, Organization for Marine Science and Technology, Nagasaki University, Taira-machi, Nagasaki, JapanDepartment of Anatomy, University of Otago, Dunedin, Otago, New ZealandDepartment of Biological Sciences and WM Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, United States of AmericaDepartment of Biological Sciences and WM Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, United States of AmericaDepartment of Anatomy, University of Otago, Dunedin, Otago, New ZealandFishes exhibit remarkably diverse, and plastic, patterns of sexual development, most striking of which is sequential hermaphroditism, where individuals readily reverse sex in adulthood. How this stunning example of phenotypic plasticity is controlled at a genetic level remains poorly understood. Several genes have been implicated in regulating sex change, yet the degree to which a conserved genetic machinery orchestrates this process has not yet been addressed. Using captive and in-the-field social manipulations to initiate sex change, combined with a comparative qPCR approach, we compared expression patterns of four candidate regulatory genes among three species of wrasses (Labridae)—a large and diverse teleost family where female-to-male sex change is pervasive, socially-cued, and likely ancestral. Expression in brain and gonadal tissues were compared among the iconic tropical bluehead wrasse (Thalassoma bifasciatum) and the temperate spotty (Notolabrus celidotus) and kyusen (Parajulus poecilepterus) wrasses. In all three species, gonadal sex change was preceded by downregulation of cyp19a1a (encoding gonadal aromatase that converts androgens to oestrogens) and accompanied by upregulation of amh (encoding anti-müllerian hormone that primarily regulates male germ cell development), and these genes may act concurrently to orchestrate ovary-testis transformation. In the brain, our data argue against a role for brain aromatase (cyp19a1b) in initiating behavioural sex change, as its expression trailed behavioural changes. However, we find that isotocin (it, that regulates teleost socio-sexual behaviours) expression correlated with dominant male-specific behaviours in the bluehead wrasse, suggesting it upregulation mediates the rapid behavioural sex change characteristic of blueheads and other tropical wrasses. However, it expression was not sex-biased in temperate spotty and kyusen wrasses, where sex change is more protracted and social groups may be less tightly-structured. Together, these findings suggest that while key components of the molecular machinery controlling gonadal sex change are phylogenetically conserved among wrasses, neural pathways governing behavioural sex change may be more variable.https://peerj.com/articles/7032.pdfProtogynous sex changeBluehead wrasseSpotty wrasseKyusen wrasseQuantitative real-time PCRSex-biased gene expression |
| spellingShingle | Jodi T. Thomas Erica V. Todd Simon Muncaster P Mark Lokman Erin L. Damsteegt Hui Liu Kiyoshi Soyano Florence Gléonnec Melissa S. Lamm John R. Godwin Neil J. Gemmell Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses PeerJ Protogynous sex change Bluehead wrasse Spotty wrasse Kyusen wrasse Quantitative real-time PCR Sex-biased gene expression |
| title | Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses |
| title_full | Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses |
| title_fullStr | Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses |
| title_full_unstemmed | Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses |
| title_short | Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses |
| title_sort | conservation and diversity in expression of candidate genes regulating socially induced female male sex change in wrasses |
| topic | Protogynous sex change Bluehead wrasse Spotty wrasse Kyusen wrasse Quantitative real-time PCR Sex-biased gene expression |
| url | https://peerj.com/articles/7032.pdf |
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