Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster

Diane Maitre,Julien Roux,Susanne Knörr,Isabelle Castro,Oliver M Selmoni,Laetitia G E Wilkins,Kenyon B Mobley,Lucas Marques Da Cunha,Marc Robinson-Rechavi,Claus Wedekind,Anshu Uppal

doi:10.1038/s41598-017-14905-9

Abstract

Fish populations can be threatened by distorted sex ratios that arise during sex differentiation. Here we describe sex differentiation in a wild grayling (Thymallus thymallus) population that suffers from distorted sex ratios. We verified that sex determination is linked to the sex determining locus (sdY) of salmonids. This allowed us to study sex-specific gene expression and gonadal development. Sex-specific gene expression could be observed during embryogenesis and was strong around hatching. About half of the fish showed immature testes around eleven weeks after fertilization. This phenotype was mostly replaced by the “testis-to-ovary” or “ovaries” phenotypes during development. The gonads of the remaining fish stayed undifferentiated until six months after fertilization. Genetic sexing revealed that fish with undifferentiated gonads were all males, who grew larger than the genetic females during the observational period. Only 12% of the genetic males showed testicular tissue six months after fertilization. We conclude that sex differentiation starts before hatching, goes through an all-male stage for both sexes (which represents a rare case of “undifferentiated” gonochoristic species that usually go through an all-female stage), and is delayed in males. During these juvenile stages males grow faster than females instead of developing their gonads.

Highlights

Fishes show a great diversity of gonadal development and differentiation that can be classified into five categories: (i) gonochoristic species with individuals developing either testes or ovaries, (ii) sequential hermaphrodites that mature as males or (iii) as females and may change sex later in life, (iv) simultaneous hermaphrodites, and (v) all-female species that reproduce gynogenetically[1,2]
We know of no example of an “undifferentiated” gonochoristic species where all individuals first develop immature testicular tissue followed by a feminization of the gonads that leads to normal ovaries in females
Fishes show a great diversity in sex determination systems that range from purely genetic to purely environmental, and different types of environmentally induced sex reversals have been described in many different orders of the teleosts[1,13]

Summary

Introduction

Fishes show a great diversity of gonadal development and differentiation that can be classified into five categories: (i) gonochoristic species with individuals developing either testes or ovaries, (ii) sequential hermaphrodites that mature as males (protandrous) or (iii) as females (protogynous) and may change sex later in life, (iv) simultaneous hermaphrodites, and (v) all-female species that reproduce gynogenetically[1,2]. Primordial germ cells are typically formed during embryonic or early larval development and subsequently differentiate into male or female gonads under the influence of genetic mechanisms and/or endocrine, environmental, or behavioural signals[1]. This process can be direct, as in the so-called “differentiated” gonochoristic species[3] where primordial germ cells develop into testicular or ovarian tissues. To detect sex-specific gene expression patterns, we extracted mRNA from embryos, hatchlings, and early larvae These time periods correspond to the onset of sexual differentiation in another salmonid, the rainbow trout (Oncorhynchus mykiss)[25]. We used histological techniques to determine sex differentiation in relation to genetic sex markers over a period of several months

Methods

Results

Conclusion