An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish
Many teleost fishes undergo natural sex change, and elucidating the physiological and molecular controls of this process offers unique opportunities not only to develop methods of controlling sex in aquaculture settings, but to better understand vertebrate sexual development more broadly. Induction...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
PeerJ Inc.
2020-11-01
|
| Series: | PeerJ |
| Subjects: | |
| Online Access: | https://peerj.com/articles/10323.pdf |
| _version_ | 1797419332329799680 |
|---|---|
| author | Alexander Goikoetxea Erin L. Damsteegt Erica V. Todd Andrew McNaughton Neil J. Gemmell P. Mark Lokman |
| author_facet | Alexander Goikoetxea Erin L. Damsteegt Erica V. Todd Andrew McNaughton Neil J. Gemmell P. Mark Lokman |
| author_sort | Alexander Goikoetxea |
| collection | DOAJ |
| description | Many teleost fishes undergo natural sex change, and elucidating the physiological and molecular controls of this process offers unique opportunities not only to develop methods of controlling sex in aquaculture settings, but to better understand vertebrate sexual development more broadly. Induction of sex change in some sequentially hermaphroditic or gonochoristic fish can be achieved in vivo through social manipulation, inhibition of aromatase activity, or steroid treatment. However, the induction of sex change in vitro has been largely unexplored. In this study, we established an in vitro culture system for ovarian explants in serum-free medium for a model sequential hermaphrodite, the New Zealand spotty wrasse (Notolabrus celidotus). This culture technique enabled evaluating the effect of various treatments with 17β-estradiol (E2), 11-ketotestosterone (11KT) or cortisol (CORT) on spotty wrasse ovarian architecture for 21 days. A quantitative approach to measuring the degree of ovarian atresia within histological images was also developed, using pixel-based machine learning software. Ovarian atresia likely due to culture was observed across all treatments including no-hormone controls, but was minimised with treatment of at least 10 ng/mL E2. Neither 11KT nor CORT administration induced proliferation of spermatogonia (i.e., sex change) in the cultured ovaries indicating culture beyond 21 days may be needed to induce sex change in vitro. The in vitro gonadal culture and analysis systems established here enable future studies investigating the paracrine role of sex steroids, glucocorticoids and a variety of other factors during gonadal sex change in fish. |
| first_indexed | 2024-03-09T06:45:49Z |
| format | Article |
| id | doaj.art-ec6aed9d31154c7881b62eabbab53ba4 |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T06:45:49Z |
| publishDate | 2020-11-01 |
| publisher | PeerJ Inc. |
| record_format | Article |
| series | PeerJ |
| spelling | doaj.art-ec6aed9d31154c7881b62eabbab53ba42023-12-03T10:36:15ZengPeerJ Inc.PeerJ2167-83592020-11-018e1032310.7717/peerj.10323An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fishAlexander Goikoetxea0Erin L. Damsteegt1Erica V. Todd2Andrew McNaughton3Neil J. Gemmell4P. Mark Lokman5Department of Anatomy, University of Otago, Dunedin, New ZealandDepartment of Zoology, University of Otago, Dunedin, New ZealandSchool of Life and Environmental Science, Deakin University, Geelong, AustraliaDepartment of Anatomy, University of Otago, Dunedin, New ZealandDepartment of Anatomy, University of Otago, Dunedin, New ZealandDepartment of Zoology, University of Otago, Dunedin, New ZealandMany teleost fishes undergo natural sex change, and elucidating the physiological and molecular controls of this process offers unique opportunities not only to develop methods of controlling sex in aquaculture settings, but to better understand vertebrate sexual development more broadly. Induction of sex change in some sequentially hermaphroditic or gonochoristic fish can be achieved in vivo through social manipulation, inhibition of aromatase activity, or steroid treatment. However, the induction of sex change in vitro has been largely unexplored. In this study, we established an in vitro culture system for ovarian explants in serum-free medium for a model sequential hermaphrodite, the New Zealand spotty wrasse (Notolabrus celidotus). This culture technique enabled evaluating the effect of various treatments with 17β-estradiol (E2), 11-ketotestosterone (11KT) or cortisol (CORT) on spotty wrasse ovarian architecture for 21 days. A quantitative approach to measuring the degree of ovarian atresia within histological images was also developed, using pixel-based machine learning software. Ovarian atresia likely due to culture was observed across all treatments including no-hormone controls, but was minimised with treatment of at least 10 ng/mL E2. Neither 11KT nor CORT administration induced proliferation of spermatogonia (i.e., sex change) in the cultured ovaries indicating culture beyond 21 days may be needed to induce sex change in vitro. The in vitro gonadal culture and analysis systems established here enable future studies investigating the paracrine role of sex steroids, glucocorticoids and a variety of other factors during gonadal sex change in fish.https://peerj.com/articles/10323.pdfOrgan cultureSex changePrevitellogenic oocyteCortisolSpotty wrasse |
| spellingShingle | Alexander Goikoetxea Erin L. Damsteegt Erica V. Todd Andrew McNaughton Neil J. Gemmell P. Mark Lokman An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish PeerJ Organ culture Sex change Previtellogenic oocyte Cortisol Spotty wrasse |
| title | An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish |
| title_full | An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish |
| title_fullStr | An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish |
| title_full_unstemmed | An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish |
| title_short | An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish |
| title_sort | in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish |
| topic | Organ culture Sex change Previtellogenic oocyte Cortisol Spotty wrasse |
| url | https://peerj.com/articles/10323.pdf |
| work_keys_str_mv | AT alexandergoikoetxea aninvitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT erinldamsteegt aninvitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT ericavtodd aninvitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT andrewmcnaughton aninvitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT neiljgemmell aninvitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT pmarklokman aninvitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT alexandergoikoetxea invitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT erinldamsteegt invitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT ericavtodd invitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT andrewmcnaughton invitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT neiljgemmell invitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish AT pmarklokman invitroovarianexplantculturesystemtoexaminesexchangeinahermaphroditicfish |