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

Clemens Falker-Gieske,Bertram Brenig,Gabriele Hörstgen-Schwark,Jens Tetens,Sebastian Herzog,Andre Franke,Henner Simianer,Ahmad Reza Sharifi,Ngoc-Thuy Ha,Shahrbanou Hosseini

doi:10.1186/s12864-019-5722-1

Clemens Falker-Gieske, Bertram Brenig + Show 8 more

Open Access

https://doi.org/10.1186/s12864-019-5722-1

Copy DOI

Abstract

BackgroundElevated 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.ResultsOur 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.ConclusionsOur 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.

Highlights

Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics
The 25.5% increase in the proportion of males under heated conditions compared to the control group suggests the induction of masculinization through the interaction between genotype and environmental factor (GxE) during sex determination (SD) and gonad differentiation
A total number of 35,119 transcripts were read in RNA sequencing (RNA-Seq) expression profiles, in which the numbers of 18,871 expressed transcripts were analysed in all experimental groups

Summary

Introduction

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. A subset of germ cells acquires the ability to operate as germ line stem cells, which later differentiate into gametes [10, 12] During this critical embryonic developmental period, the loss or decrease in the number of PGCs may cause by increased water temperatures leads to masculinization [11, 13, 14]. E.g. caused by climate change, may induce male-biased populations, leading to an elevated risk of extinction in thermosensitive fish populations in nature [16]

Methods

Results

Discussion

Conclusion