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Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard

BACKGROUND: In some vertebrate species, gene-environment interactions can determine sex, driving bipotential gonads to differentiate into either ovaries or testes. In the central bearded dragon (Pogona vitticeps), the genetic influence of sex chromosomes (ZZ/ZW) can be overridden by high incubation...

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Autores principales: Whiteley, Sarah L., Holleley, Clare E., Georges, Arthur
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9034607/
https://www.ncbi.nlm.nih.gov/pubmed/35459109
http://dx.doi.org/10.1186/s12864-022-08544-2
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author Whiteley, Sarah L.
Holleley, Clare E.
Georges, Arthur
author_facet Whiteley, Sarah L.
Holleley, Clare E.
Georges, Arthur
author_sort Whiteley, Sarah L.
collection PubMed
description BACKGROUND: In some vertebrate species, gene-environment interactions can determine sex, driving bipotential gonads to differentiate into either ovaries or testes. In the central bearded dragon (Pogona vitticeps), the genetic influence of sex chromosomes (ZZ/ZW) can be overridden by high incubation temperatures, causing ZZ male to female sex reversal. Previous research showed ovotestes, a rare gonadal phenotype with traits of both sexes, develop during sex reversal, leading to the hypothesis that sex reversal relies on high temperature feminisation to outcompete the male genetic cue. To test this, we conducted temperature switching experiments at key developmental stages, and analysed the effect on gonadal phenotypes using histology and transcriptomics. RESULTS: We found sexual fate is more strongly influenced by the ZZ genotype than temperature. Any exposure to low temperatures (28 °C) caused testes differentiation, whereas sex reversal required longer exposure to high temperatures. We revealed ovotestes exist along a spectrum of femaleness to male-ness at the transcriptional level. We found inter-individual variation in gene expression changes following temperature switches, suggesting both genetic sensitivity to, and the timing and duration of the temperature cue influences sex reversal. CONCLUSIONS: These findings bring new insights to the mechanisms underlying sex reversal, improving our understanding of thermosensitive sex systems in vertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08544-2.
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spelling pubmed-90346072022-04-24 Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard Whiteley, Sarah L. Holleley, Clare E. Georges, Arthur BMC Genomics Research Article BACKGROUND: In some vertebrate species, gene-environment interactions can determine sex, driving bipotential gonads to differentiate into either ovaries or testes. In the central bearded dragon (Pogona vitticeps), the genetic influence of sex chromosomes (ZZ/ZW) can be overridden by high incubation temperatures, causing ZZ male to female sex reversal. Previous research showed ovotestes, a rare gonadal phenotype with traits of both sexes, develop during sex reversal, leading to the hypothesis that sex reversal relies on high temperature feminisation to outcompete the male genetic cue. To test this, we conducted temperature switching experiments at key developmental stages, and analysed the effect on gonadal phenotypes using histology and transcriptomics. RESULTS: We found sexual fate is more strongly influenced by the ZZ genotype than temperature. Any exposure to low temperatures (28 °C) caused testes differentiation, whereas sex reversal required longer exposure to high temperatures. We revealed ovotestes exist along a spectrum of femaleness to male-ness at the transcriptional level. We found inter-individual variation in gene expression changes following temperature switches, suggesting both genetic sensitivity to, and the timing and duration of the temperature cue influences sex reversal. CONCLUSIONS: These findings bring new insights to the mechanisms underlying sex reversal, improving our understanding of thermosensitive sex systems in vertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08544-2. BioMed Central 2022-04-22 /pmc/articles/PMC9034607/ /pubmed/35459109 http://dx.doi.org/10.1186/s12864-022-08544-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visithttp://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Whiteley, Sarah L.
Holleley, Clare E.
Georges, Arthur
Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
title Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
title_full Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
title_fullStr Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
title_full_unstemmed Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
title_short Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
title_sort developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9034607/
https://www.ncbi.nlm.nih.gov/pubmed/35459109
http://dx.doi.org/10.1186/s12864-022-08544-2
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