Abstract

Sexual reproduction is widespread among eukaryotes, and the sex-determining processes vary greatly among species. While genetic sex determination (GSD) has been intensively described in bilaterian species, no example has yet been recorded among non-bilaterians. However, the quasi-ubiquitous repartition of GSD among multicellular species suggests that similar evolutionary forces can promote this system, and that these forces could occur also in non-bilaterians. Studying sex determination across the range of Metazoan diversity is indeed important to understand better the evolution of this mechanism and its lability. We tested the existence of sex-linked genes in the gonochoric red coral (Corallium rubrum, Cnidaria) using restriction site-associated DNA sequencing. We analysed 27 461 single nucleotide polymorphisms (SNPs) in 354 individuals from 12 populations including 53 that were morphologically sexed. We found a strong association between the allele frequencies of 472 SNPs and the sex of individuals, suggesting an XX/XY sex-determination system. This result was confirmed by the identification of 435 male-specific loci. An independent test confirmed that the amplification of these loci enabled us to identify males with absolute certainty. This is the first demonstration of a GSD system among non-bilaterian species and a new example of its convergence in multicellular eukaryotes.

Highlights

  • Sexual reproduction is ubiquitous among eukaryotes [1], and there is a wealth of literature on the evolutionary advantages of sex [2]

  • The sexual identity of individuals is defined by sex-determination systems, going from purely genetic sex determination (GSD), to purely environmental sex determination (ESD) where the same genotype can produce both male and female phenotypes depending on environmental conditions [3]

  • This gene was neither a sex-specific marker nor a sex-linked marker, which remains compatible with a role in sexual differentiation. The exploration both of sex-linked polymorphisms and of sex-specific loci enabled us to identify an XX/XY genetic sex-determination system in the red coral. This is the first time such an identification has been made for non-bilaterian species, and is a new example of the evolution of GSD in multicellular organisms [3,39]

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Summary

Introduction

Sexual reproduction is ubiquitous among eukaryotes [1], and there is a wealth of literature on the evolutionary advantages of sex [2]. The quasi-ubiquitous repartition of GSD among eukaryotes suggests that similar evolutionary forces repeatedly led to the evolution of GSD, and these forces could occur in non-bilaterians. This lack of evidence of GSD in non-bilaterians is probably the consequence of a reduced number of model organisms in these groups, and sometimes of the difficulty to identify separate sexes. Studying sex determination along the range of Metazoan diversity is important to understand better the evolution of this mechanism and its lability. Understanding the ancestral state of sex-determination systems in Metazoans requires studying them in the main branches of the phylogenetic tree

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