Abstract
Wolbachia is an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification of Wolbachia in certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematode Wolbachia has attracted great interest. The obligate symbiosis in filariae, which renders infected species susceptible to antibiotic chemotherapy, was held to be distinct from the Wolbachia-arthropod relationship, typified by reproductive parasitism. While co-evolutionary signatures in Wolbachia-arthropod symbioses are generally weak, reflecting horizontal transmission events, strict co-evolution between filariae and Wolbachia has been reported previously. However, the absence of close outgroups for phylogenetic studies prevented the determination of which host group originally acquired Wolbachia. Here, we present the largest co-phylogenetic analysis of Wolbachia in filariae performed to date including: (i) a screening and an updated phylogeny of Wolbachia; (ii) a co-phylogenetic analysis; and (iii) a hypothesis on the acquisition of Wolbachia infection. First, our results show a general overestimation of Wolbachia occurrence 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 with Wolbachia in supergroups C and J. In other filarial clades, harbouring Wolbachia supergroups D and F, horizontal acquisitions and secondary losses are common. Finally, our results suggest that supergroup C is the basal Wolbachia clade within the Ecdysozoa. This hypothesis on the origin of Wolbachia would change drastically our understanding of Wolbachia evolution.
Highlights
Wolbachia (Rickettsiales, Anaplasmataceae) are α-proteobacteria closely related to Ehrlichia and Anaplasma species
They are vertically transmitted from females to offspring. This bacterium induces a large range of phenotypes in its hosts, varying from mutualism, including obligate dependencies for reproduction and long-term survival (Hosokawa et al, 2010; Zug & Hammerstein, 2015; Hoerauf et al, 2003); to parasitism by interfering with host reproduction (Werren, Baldo & Clark, 2008)
The spread of Wolbachia via cytoplasmic incompatibility, male killing, feminization and induction of parthenogenesis can have a major impact on the evolution of arthropod host populations, and in some cases, may drive speciation (Rokas, 2000; Telschow et al, 2007)
Summary
Wolbachia (Rickettsiales, Anaplasmataceae) are α-proteobacteria closely related to Ehrlichia and Anaplasma species. From 1999 to 2015, a multiplication of supergroup classifications occurred, with 10 clades identified that exclusively infect arthropods (supergroups E, G, H, I, K, M, N, O, P and Q) (Augustinos et al, 2011; Bing et al, 2014; Bordenstein & Rosengaus, 2005; Czarnetzki & Tebbe, 2004; Dittmar & Whiting, 2004; Glowska et al, 2015; Ros et al, 2009; Rowley, Raven & McGraw, 2004; Vandekerckhove et al, 1999; Wang et al, 2014); one infecting filariae (supergroup J) (Casiraghi et al, 2004); one identified in the plant parasite nematode Radopholus similis (Tylenchida) (supergroup L) (Haegeman et al, 2009); and supergroup F, which is apparently unique in infecting both arthropods and filariae (Casiraghi et al, 2001b; Lo et al, 2002) These phylogenetic analyses led to Wolbachia classification gradually increasing in complexity from single gene analysis (Sironi et al, 1995; Werren, Zhang & Guo, 1995) to multi-locus methods (Baldo et al, 2006b; Bordenstein et al, 2009; Casiraghi et al, 2001a; Casiraghi et al, 2005; Lefoulon et al, 2012). We apply a new approach to the question of initial acquisition of Wolbachia within the Ecdysozoa
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