Ghosts of symbionts past: The hidden history of the dynamic association between filarial nematodes and their Wolbachia endosymbionts
Many, but not all, parasitic filarial nematodes (Onchocercidae) carry intracellular, maternally-transmitted, alphaproteobacterial Wolbachia symbionts. The association between filarial nematodes and Wolbachia is often portrayed as mutualist, where the nematode is reliant on Wolbachia for an essential but unknown service. Wolbachia are targets for anti-filarial chemotherapeutic interventions for human disease. Wolbachia of Onchocercidae derive from four of the major supergroups (C, D, F and J) defined within the genus. We explored the evolutionary history of the filarial nematode-Wolbachia symbiosis in twenty-two nematode species, sixteen of which have current Wolbachia infections, by screening the nematode nuclear genome sequences for nuclear Wolbachia transfers, fragments of the Wolbachia genome that have been inserted into the nuclear genome. We identified Wolbachia insertions in five of the six species that have no current Wolbachia infection, showing they have previously had and have now lost Wolbachia infections. In currently-infected species we found a diversity of origins of the insertions, including many cases where they derived from a different supergroup to the current live infection. Mapping the origins of the insertions onto the filarial nematode phylogeny we derive a complex model of evolution of Wolbachia symbiosis. The history of association between Wolbachia and onchocercid nematodes includes not only cospeciation, as would be expected from a mutualist symbiosis, but also loss (in the five Wolbachia-free species), frequent symbiont replacement, and dual infection. This dynamic pattern is challenging to models that assume host-symbiont mutualism.
Emmelien Vancaester, Guy R Oldrieve, Alex Reid, Georgios Koutsovoulos, Dominik R Laetsch, Benjamin L Makepeace, Vincent Tanya, Sven Poppert, Jürgen Krücken, Adrian Wolstenholme, Mark Blaxter. G3 (Bethesda). 2025 Oct 1:jkaf226. doi: 10.1093/g3journal/jkaf226.


