Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)

Abstract Background Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics. These changes are one important ecological consequence, contributing to the risk of extinction in small...

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Main Authors: Shahrbanou Hosseini, Ngoc-Thuy Ha, Henner Simianer, Clemens Falker-Gieske, Bertram Brenig, Andre Franke, Gabriele Hörstgen-Schwark, Jens Tetens, Sebastian Herzog, Ahmad Reza Sharifi
Format: Article
Language:English
Published: BMC 2019-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5722-1
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spelling doaj-bf8e52f62caa491cbea1735bb15958612020-11-25T02:02:23ZengBMCBMC Genomics1471-21642019-05-0120111710.1186/s12864-019-5722-1Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)Shahrbanou Hosseini0Ngoc-Thuy Ha1Henner Simianer2Clemens Falker-Gieske3Bertram Brenig4Andre Franke5Gabriele Hörstgen-Schwark6Jens Tetens7Sebastian Herzog8Ahmad Reza Sharifi9Department of Animal Sciences, University of GoettingenDepartment of Animal Sciences, University of GoettingenDepartment of Animal Sciences, University of GoettingenDepartment of Animal Sciences, University of GoettingenDepartment of Animal Sciences, University of GoettingenInstitute of Clinical Molecular Biology, Christian-Albrechts-UniversityDepartment of Animal Sciences, University of GoettingenDepartment of Animal Sciences, University of GoettingenMax Planck Institute for Dynamics and Self-OrganizationDepartment of Animal Sciences, University of GoettingenAbstract Background Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics. These changes are one important ecological consequence, contributing to the risk of extinction in small and inbred fish populations under natural conditions, due to male-biased sex ratio. Here we investigated the effect of elevated water temperature during embryogenesis on sex ratio and sex-biased gene expression profiles between two different tissues, namely gonad and caudal fin of adult zebrafish males and females, to gain new insights into the molecular mechanisms underlying sex determination (SD) and colour patterning related to sexual attractiveness. Results Our study demonstrated sex ratio imbalances with 25.5% more males under high-temperature condition, resulting from gonadal masculinization. The result of transcriptome analysis showed a significantly upregulated expression of male SD genes (e.g. dmrt1, amh, cyp11c1 and sept8b) and downregulation of female SD genes (e.g. zp2.1, vtg1, cyp19a1a and bmp15) in male gonads compared to female gonads. Contrary to expectations, we found highly differential expression of colour pattern (CP) genes in the gonads, suggesting the ‘neofunctionalisation’ of those genes in the zebrafish reproduction system. However, in the caudal fin, no differential expression of CP genes was identified, suggesting the observed differences in colouration between males and females in adult fish may be due to post-transcriptional regulation of key enzymes involved in pigment synthesis and distribution. Conclusions Our study demonstrates male-biased sex ratio under high temperature condition and support a polygenic SD (PSD) system in laboratory zebrafish. We identify a subset of pathways (tight junction, gap junction and apoptosis), enriched for SD and CP genes, which appear to be co-regulated in the same pathway, providing evidence for involvement of those genes in the regulation of phenotypic sexual dimorphism in zebrafish.http://link.springer.com/article/10.1186/s12864-019-5722-1ZebrafishTemperatureEmbryogenesisSex ratioSex determinationColour pattern
collection DOAJ
language English
format Article
sources DOAJ
author Shahrbanou Hosseini
Ngoc-Thuy Ha
Henner Simianer
Clemens Falker-Gieske
Bertram Brenig
Andre Franke
Gabriele Hörstgen-Schwark
Jens Tetens
Sebastian Herzog
Ahmad Reza Sharifi
spellingShingle Shahrbanou Hosseini
Ngoc-Thuy Ha
Henner Simianer
Clemens Falker-Gieske
Bertram Brenig
Andre Franke
Gabriele Hörstgen-Schwark
Jens Tetens
Sebastian Herzog
Ahmad Reza Sharifi
Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
BMC Genomics
Zebrafish
Temperature
Embryogenesis
Sex ratio
Sex determination
Colour pattern
author_facet Shahrbanou Hosseini
Ngoc-Thuy Ha
Henner Simianer
Clemens Falker-Gieske
Bertram Brenig
Andre Franke
Gabriele Hörstgen-Schwark
Jens Tetens
Sebastian Herzog
Ahmad Reza Sharifi
author_sort Shahrbanou Hosseini
title Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_short Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_full Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_fullStr Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_full_unstemmed Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_sort genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (danio rerio)
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-05-01
description Abstract Background Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics. These changes are one important ecological consequence, contributing to the risk of extinction in small and inbred fish populations under natural conditions, due to male-biased sex ratio. Here we investigated the effect of elevated water temperature during embryogenesis on sex ratio and sex-biased gene expression profiles between two different tissues, namely gonad and caudal fin of adult zebrafish males and females, to gain new insights into the molecular mechanisms underlying sex determination (SD) and colour patterning related to sexual attractiveness. Results Our study demonstrated sex ratio imbalances with 25.5% more males under high-temperature condition, resulting from gonadal masculinization. The result of transcriptome analysis showed a significantly upregulated expression of male SD genes (e.g. dmrt1, amh, cyp11c1 and sept8b) and downregulation of female SD genes (e.g. zp2.1, vtg1, cyp19a1a and bmp15) in male gonads compared to female gonads. Contrary to expectations, we found highly differential expression of colour pattern (CP) genes in the gonads, suggesting the ‘neofunctionalisation’ of those genes in the zebrafish reproduction system. However, in the caudal fin, no differential expression of CP genes was identified, suggesting the observed differences in colouration between males and females in adult fish may be due to post-transcriptional regulation of key enzymes involved in pigment synthesis and distribution. Conclusions Our study demonstrates male-biased sex ratio under high temperature condition and support a polygenic SD (PSD) system in laboratory zebrafish. We identify a subset of pathways (tight junction, gap junction and apoptosis), enriched for SD and CP genes, which appear to be co-regulated in the same pathway, providing evidence for involvement of those genes in the regulation of phenotypic sexual dimorphism in zebrafish.
topic Zebrafish
Temperature
Embryogenesis
Sex ratio
Sex determination
Colour pattern
url http://link.springer.com/article/10.1186/s12864-019-5722-1
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