Breakdown of coevolution between symbiotic bacteriaWolbachiaand their filarial hosts

Abstract

Wolbachiais an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification ofWolbachiain certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematodeWolbachiahas attracted great interest. The obligate symbiosis in filariae, which renders infected species susceptible to antibiotic chemotherapy, was held to be distinct from theWolbachia-arthropod relationship, typified by reproductive parasitism. While co-evolutionary signatures inWolbachia-arthropod symbioses are generally weak, reflecting horizontal transmission events, strict co-evolution between filariae andWolbachiahas been reported previously. However, the absence of close outgroups for phylogenetic studies prevented the determination of which host group originally acquiredWolbachia. Here, we present the largest co-phylogenetic analysis ofWolbachiain filariae performed to date including: (i) a screening and an updated phylogeny ofWolbachia; (ii) a co-phylogenetic analysis; and (iii) a hypothesis on the acquisition ofWolbachiainfection. First, our results show a general overestimation ofWolbachiaoccurrence and support the hypothesis of an ancestral absence of infection in the nematode phylum. The accuracy of supergroup J is also underlined. Second, although a global pattern of coevolution remains, the signal is derived predominantly from filarial clades associated withWolbachiain supergroups C and J. In other filarial clades, harbouringWolbachiasupergroups D and F, horizontal acquisitions and secondary losses are common. Finally, our results suggest that supergroup C is the basalWolbachiaclade within the Ecdysozoa. This hypothesis on the origin ofWolbachiawould change drastically our understanding ofWolbachiaevolution.