Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii

Abstract Temperature-dependent sex determination (TSD) is a mechanism in which environmental temperature, rather than innate zygotic genotype, determines the fate of sexual differentiation during embryonic development. Reeves’ turtle (also known as the Chinese three-keeled pond turtle, Mauremys reev...

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Main Authors: Hiroshi Akashi, Manami Kubota, Hibiki Yamamoto, Kaori Miyaoku, Genki Yamagishi, Shinichi Miyagawa
Format: Article
Language:English
Published: Nature Portfolio 2022-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-15515-w
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author Hiroshi Akashi
Manami Kubota
Hibiki Yamamoto
Kaori Miyaoku
Genki Yamagishi
Shinichi Miyagawa
author_facet Hiroshi Akashi
Manami Kubota
Hibiki Yamamoto
Kaori Miyaoku
Genki Yamagishi
Shinichi Miyagawa
author_sort Hiroshi Akashi
collection DOAJ
description Abstract Temperature-dependent sex determination (TSD) is a mechanism in which environmental temperature, rather than innate zygotic genotype, determines the fate of sexual differentiation during embryonic development. Reeves’ turtle (also known as the Chinese three-keeled pond turtle, Mauremys reevesii) exhibits TSD and is the only species whose genome has been determined in Geoemydidae to date. Thus, M. reevesii occupy phylogenetically important position for the study of TSD and can be compared to other TSD species to elucidate the underlying molecular mechanism of this process. Nevertheless, neither embryogenesis nor gonadogenesis has been described in this species. Therefore, herein, we investigated the chronology of normal embryonic development and gonadal structures in M. reevesii under both female- and male-producing incubation temperatures (FPT 31 °C or MPT 26 °C, respectively). External morphology remains indistinct between the two temperature regimes throughout the studied embryonic stages. However, the gonadal ridges present on the mesonephros at stage 16 develop and sexually differentiate at FPT and MPT. Ovarian and testicular structures begin to develop at stages 18–19 at FPT and stages 20–21 at MPT, respectively, and thus, the sexual differentiation of gonadal structures began earlier in the embryos at FPT than at MPT. Our results suggest that temperature sensitive period, at which the gonadal structures remain sexually undifferentiated, spans from stage 16 (or earlier) to stages 18–19 at FPT and to stages 20–21 at MPT. Understanding the temperature-dependent differentiation in gonadal structures during embryonic development is a prerequisite for investigating molecular basis underlying TSD. Thus, the result of the present study will facilitate further developmental studies on TSD in M. reevesii.
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spelling doaj.art-2a576922b48a4273a0684385ce4cc76a2022-12-22T01:00:02ZengNature PortfolioScientific Reports2045-23222022-07-0112111110.1038/s41598-022-15515-wChronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesiiHiroshi Akashi0Manami Kubota1Hibiki Yamamoto2Kaori Miyaoku3Genki Yamagishi4Shinichi Miyagawa5Department of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of ScienceDepartment of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of ScienceDepartment of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of ScienceDepartment of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of ScienceDepartment of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of ScienceDepartment of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of ScienceAbstract Temperature-dependent sex determination (TSD) is a mechanism in which environmental temperature, rather than innate zygotic genotype, determines the fate of sexual differentiation during embryonic development. Reeves’ turtle (also known as the Chinese three-keeled pond turtle, Mauremys reevesii) exhibits TSD and is the only species whose genome has been determined in Geoemydidae to date. Thus, M. reevesii occupy phylogenetically important position for the study of TSD and can be compared to other TSD species to elucidate the underlying molecular mechanism of this process. Nevertheless, neither embryogenesis nor gonadogenesis has been described in this species. Therefore, herein, we investigated the chronology of normal embryonic development and gonadal structures in M. reevesii under both female- and male-producing incubation temperatures (FPT 31 °C or MPT 26 °C, respectively). External morphology remains indistinct between the two temperature regimes throughout the studied embryonic stages. However, the gonadal ridges present on the mesonephros at stage 16 develop and sexually differentiate at FPT and MPT. Ovarian and testicular structures begin to develop at stages 18–19 at FPT and stages 20–21 at MPT, respectively, and thus, the sexual differentiation of gonadal structures began earlier in the embryos at FPT than at MPT. Our results suggest that temperature sensitive period, at which the gonadal structures remain sexually undifferentiated, spans from stage 16 (or earlier) to stages 18–19 at FPT and to stages 20–21 at MPT. Understanding the temperature-dependent differentiation in gonadal structures during embryonic development is a prerequisite for investigating molecular basis underlying TSD. Thus, the result of the present study will facilitate further developmental studies on TSD in M. reevesii.https://doi.org/10.1038/s41598-022-15515-w
spellingShingle Hiroshi Akashi
Manami Kubota
Hibiki Yamamoto
Kaori Miyaoku
Genki Yamagishi
Shinichi Miyagawa
Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii
Scientific Reports
title Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii
title_full Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii
title_fullStr Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii
title_full_unstemmed Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii
title_short Chronology of embryonic and gonadal development in the Reeves’ turtle, Mauremys reevesii
title_sort chronology of embryonic and gonadal development in the reeves turtle mauremys reevesii
url https://doi.org/10.1038/s41598-022-15515-w
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