Frequent intertrophic transmission of Wolbachia by parasitism but not predation

Abstract

Wolbachia is one of the most pervasive symbionts, estimated to infect ~50% of arthropod species. It is primarily transmitted vertically, inducing a variety of fascinating reproductive manipulations to promote its spread within host populations. However, incongruences between host and Wolbachia phylogenies indicate substantial horizontal transmissions, the mechanisms of which are largely unexplored. By systematically analyzing Wolbachia surface protein (wsp) sequences on NCBI, we found that parasitism, not predation, is the primary route of intertropical Wolbachia transmission. This conclusion held after accounting for sampling bias. One example of frequent Wolbachia transfers is between egg parasitoid wasps, Trichogramma, and their lepidopteran hosts. Moreover, both bioinformatics and experimental results showed that Wolbachia from the parasitoid wasp Encarsia formosa can be transmitted to its whitefly host Bemisia tabaci, through unsuccessful parasitism. Once En. formosa Wolbachia is transferred to whiteflies, it can be vertically transmitted within whiteflies and induce fitness costs. To our knowledge, this is the first compelling evidence that Wolbachia can be transmitted from parasitoid wasps to their hosts, revealing the bidirectional nature of Wolbachia transfers between parasitoids and their hosts. Overall, our findings enrich the current understanding of the horizontal transmission of Wolbachia and shed new light on its ecology and evolution.