Final Report Summary - ENDOSEXDET (The impact of endosymbionts on the evolution of host sex determination mechanisms)
Animals have been continuously involved in complex interactions with microorganisms during their evolution, the most intimate of which is endosymbiosis, a type of symbiosis in which a microbial partner lives inside its host cells. Endosymbiosis has played a key role in the emergence of major life forms on Earth and in the generation of biological diversity. However, appreciation of endosymbiosis as an important source of evolutionary novelty has developed relatively recently. In the EndoSexDet project, we investigate a critical evolutionary process influenced by bacterial endosymbionts: the mechanisms of sex determination of their animal hosts. In animals, sex determination is generally under the control of genes located on sex chromosomes. However, in some species, sex determination can be affected by inherited bacterial endosymbionts, a phenomenon known as cytoplasmic sex determination. Distorting host sex ratio towards females may be advantageous for endosymbionts because they are predominantly transmitted through female lines but not through males. However, very few systems have been analyzed in detail and there is no extensive empirical evidence of how endosymbionts can shape sex-determining systems. In the isopod crustacean Armadillidium vulgare, genetic sex determination follows female heterogamety (males have ZZ sex chromosomes and females have ZW sex chromosomes). However, many A. vulgare populations harbor Wolbachia endosymbionts which can convert individuals with male sex chromosomes (ZZ) into sexually functional females. Sex determination of these isopods is therefore under the control of Wolbachia in infected populations: individuals inheriting Wolbachia develop as females (~90%) whereas males are uninfected individuals (~10%). Other sex-determining factors have been identified in A. vulgare, including a feminizing agent (termed f element) which has been hypothesized to be a fragment of the Wolbachia genome carrying feminization information inserted into the host nuclear genome, and an autosomal masculinizing gene (termed M gene) which can restore the male sex in the presence of the f element. Thus, sex determination mechanisms in A. vulgare are highly dynamic and under the influence of Wolbachia endosymbionts. In this context, the aims of EndoSexDet are to uncover the molecular genetic basis and evolutionary history of feminization by Wolbachia, the f element and the “female gene” carried by the W female sex chromosome, and masculinisation by the M gene. The latest developments of molecular genetics technologies now make it possible to address these exciting questions. Using high-throughput DNA sequencing and bioinformatics tools, we have identified candidate genes for feminization induced by Wolbachia. We also identified the f element as a piece of the Wolbachia genome that has been transferred to the A. vulgare nucleus and is in perfect linkage with the female sex. We also sequenced the genome of an A. vulgare female to locate the W female sex chromosome and identify the M gene. With this project, we aimed at shedding light on the largely underappreciated influence of prokaryotic endosymbionts on a fundamental eukaryotic biological process: the evolution of sex determination mechanisms.