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Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ

SIMPLE SUMMARY: This study maps critical events of gonadogenesis in the live-bearing fish Gambusia holbrooki. Significantly, it provides the first evidence for primary gonochorism, the transition of an embryonically bi-lobed gonad to a mono-lobed organ, as occurs in adults and the dimorphically prog...

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Autores principales: Razmi, Komeil, Tran, Ngoc Kim, Patil, Jawahar G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10215382/
https://www.ncbi.nlm.nih.gov/pubmed/37237542
http://dx.doi.org/10.3390/biology12050731
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author Razmi, Komeil
Tran, Ngoc Kim
Patil, Jawahar G.
author_facet Razmi, Komeil
Tran, Ngoc Kim
Patil, Jawahar G.
author_sort Razmi, Komeil
collection PubMed
description SIMPLE SUMMARY: This study maps critical events of gonadogenesis in the live-bearing fish Gambusia holbrooki. Significantly, it provides the first evidence for primary gonochorism, the transition of an embryonically bi-lobed gonad to a mono-lobed organ, as occurs in adults and the dimorphically programmed onset of sex differentiation in this species. The outcomes are significant in basic biology and are applicable for developing control options for this notorious pest fish. ABSTRACT: Despite their uniqueness, the ontogeny and differentiation of the single-lobed gonads in the poeciliids are very poorly understood. To address this, we employed both cellular and molecular approaches to systematically map the development of the testes and ovary in Gambusia holbrooki from pre-parturition to adulthood, encompassing well over 19 developmental stages. The results show that putative gonads form prior to the completion of somitogenesis in this species, a comparatively early occurrence among teleosts. Remarkably, the species recapitulates the typical bi-lobed origin of the gonads during early development that later undergoes steric metamorphosis to form a single-lobed organ. Thereafter, the germ cells undergo mitotic proliferation in a sex-dependent manner before the acquisition of the sexual phenotype. The differentiation of the ovary preceded that of the testes, which occurred before parturition, where the genetic females developed meiotic primary oocytes stage I, indicating ovarian differentiation. However, genetic males showed gonial stem cells in nests with slow mitotic proliferation at the same developmental stage. Indeed, the first signs of male differentiation were obvious only post-parturition. The expression pattern of the gonadosoma markers foxl2, cyp19a1a, amh and dmrt1 in pre- and post-natal developmental stages were consistent with morphological changes in early gonad; they were activated during embryogenesis, followed by the onset of gonad formation, and a sex-dimorphic expression pattern concurrent with sex differentiation of the ovary (foxl2, cyp19a1a) and testes (amh and dmrt1). In conclusion, this study documents for the first time the underlying events of gonad formation in G. holbrooki and shows that this occurs relatively earlier than those previously described for ovi- and viviparous fish species, which may contribute to its reproductive and invasive prowess.
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spelling pubmed-102153822023-05-27 Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ Razmi, Komeil Tran, Ngoc Kim Patil, Jawahar G. Biology (Basel) Article SIMPLE SUMMARY: This study maps critical events of gonadogenesis in the live-bearing fish Gambusia holbrooki. Significantly, it provides the first evidence for primary gonochorism, the transition of an embryonically bi-lobed gonad to a mono-lobed organ, as occurs in adults and the dimorphically programmed onset of sex differentiation in this species. The outcomes are significant in basic biology and are applicable for developing control options for this notorious pest fish. ABSTRACT: Despite their uniqueness, the ontogeny and differentiation of the single-lobed gonads in the poeciliids are very poorly understood. To address this, we employed both cellular and molecular approaches to systematically map the development of the testes and ovary in Gambusia holbrooki from pre-parturition to adulthood, encompassing well over 19 developmental stages. The results show that putative gonads form prior to the completion of somitogenesis in this species, a comparatively early occurrence among teleosts. Remarkably, the species recapitulates the typical bi-lobed origin of the gonads during early development that later undergoes steric metamorphosis to form a single-lobed organ. Thereafter, the germ cells undergo mitotic proliferation in a sex-dependent manner before the acquisition of the sexual phenotype. The differentiation of the ovary preceded that of the testes, which occurred before parturition, where the genetic females developed meiotic primary oocytes stage I, indicating ovarian differentiation. However, genetic males showed gonial stem cells in nests with slow mitotic proliferation at the same developmental stage. Indeed, the first signs of male differentiation were obvious only post-parturition. The expression pattern of the gonadosoma markers foxl2, cyp19a1a, amh and dmrt1 in pre- and post-natal developmental stages were consistent with morphological changes in early gonad; they were activated during embryogenesis, followed by the onset of gonad formation, and a sex-dimorphic expression pattern concurrent with sex differentiation of the ovary (foxl2, cyp19a1a) and testes (amh and dmrt1). In conclusion, this study documents for the first time the underlying events of gonad formation in G. holbrooki and shows that this occurs relatively earlier than those previously described for ovi- and viviparous fish species, which may contribute to its reproductive and invasive prowess. MDPI 2023-05-16 /pmc/articles/PMC10215382/ /pubmed/37237542 http://dx.doi.org/10.3390/biology12050731 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Razmi, Komeil
Tran, Ngoc Kim
Patil, Jawahar G.
Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ
title Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ
title_full Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ
title_fullStr Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ
title_full_unstemmed Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ
title_short Gonad Ontogeny and Sex Differentiation in a Poeciliid, Gambusia holbrooki: Transition from a Bi- to a Mono-Lobed Organ
title_sort gonad ontogeny and sex differentiation in a poeciliid, gambusia holbrooki: transition from a bi- to a mono-lobed organ
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10215382/
https://www.ncbi.nlm.nih.gov/pubmed/37237542
http://dx.doi.org/10.3390/biology12050731
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