Wolbachia are widespread endosymbionts found in a large variety of arthropods. While these bacteria are generally transmitted vertically and exhibit weak virulence in their native hosts, a growing number of studies suggests that horizontal transfers of Wolbachia to new host species also occur frequently in nature. In transfer situations, virulence variations can be predicted since hosts and symbionts are not adapted to each other. Here, we describe a situation where a Wolbachia strain (wVulC) becomes a pathogen when transfected from its native terrestrial isopod host species (Armadillidium vulgare) to another species (Porcellio d. dilatatus). Such transfer of wVulC kills all recipient animals within 75 days. Before death, animals suffer symptoms such as growth slowdown and nervous system disorders. Neither those symptoms nor mortalities were observed after injection of wVulC into its native host A. vulgare. Analyses of wVulC's densities in main organs including Central Nervous System (CNS) of both naturally infected A. vulgare and transfected P. d. dilatatus and A. vulgare individuals revealed a similar pattern of host colonization suggesting an overall similar resistance of both host species towards this bacterium. However, for only P. d. dilatatus, we observed drastic accumulations of autophagic vesicles and vacuoles in the nerve cells and adipocytes of the CNS from individuals infected by wVulC. The symptoms and mortalities could therefore be explained by this huge autophagic response against wVulC in P. d. dilatatus cells that is not triggered in A. vulgare. Our results show that Wolbachia (wVulC) can lead to a pathogenic interaction when transferred horizontally into species that are phylogenetically close to their native hosts. This change in virulence likely results from the autophagic response of the host, strongly altering its tolerance to the symbiont and turning it into a deadly pathogen.

Sex determination systems are highly variable in many taxa, sometimes even between closely related species. Yet the number and direction of transitions between these systems have seldom been characterized, and the underlying mechanisms are still poorly understood. Here we generated transcriptomes for 19 species of terrestrial isopod crustaceans, many of which are infected by Wolbachia bacterial endosymbionts. Using 88 single-copy orthologous genes, we reconstructed a fully resolved and dated phylogeny of terrestrial isopods. An original approach involving crossings of sex-reversed individuals allowed us to characterize the heterogametic systems of five species (one XY/XX and four ZW/ZZ). Mapping of these and previously known heterogametic systems onto the terrestrial isopod phylogeny revealed between 3 and 13 transitions of sex determination systems during the evolution of these taxa, most frequently from female to male heterogamety. Our results support that WW individuals are viable in many species, suggesting sex chromosomes are at an incipient stage of their evolution. Together, these data are consistent with the hypothesis that nucleo-cytoplasmic conflicts generated by Wolbachia endosymbionts triggered recurrent turnovers of sex determination systems in terrestrial isopods. They further establish terrestrial isopods as a model to study evolutionary transitions in sex determination systems and pave the way to molecularly characterize these systems.