Establishing drivers of the heritable symbiont ‘pandemic’

If you see an insect in your garden, the chances are that it carries one or more partner bacteria (‘heritable symbionts’) which pass from a female insect to her offspring. These ‘small things’ represent major hidden players in insect biology, providing key services such as protection against enemies, nutrient synthesis, and desiccation tolerance. These services may define the niche of their host species and drive the dynamics of natural enemy/host interactions. Further, their innovations drive insect evolution, for instance fuelling the radiation of the lineages. Whilst the importance of heritable symbionts for insect biology and ecology is understood, the forces that have enabled them to impact so many host species are not. For instance, the microbe Wolbachia is present in over 40% of species - but we simply do not understand how so many insect species came to carry it. Our project’s overarching challenge is to understand how these symbioses – that define insect biology – became so common. New heritable symbiont/host interactions are established when an existing symbiont moves from its native host species to a new one. These ‘host shifts’ involve two processes – transfer of the microbe into a novel host, and compatibility with that host such that a stable symbiosis is formed both initially, and in the face of onward environmental stress. Problem 1: How do symbionts transfer to new hosts? Symbiont introduction to a new host is thought to occur most commonly when a parasite develops inside an insect, such that each party is exposed to the symbionts of the other. However, this process has a key barrier: it requires the insect to survive parasite attack. We hypothesize the common phenomenon of symbiont-mediated protection – where partner microbes kill developing parasite larvae – is the missing link enabling transfer of symbionts from parasite to host. We will test this hypothesis for Wolbachia transfer from parasitic wasp to fruit flies. We have shown flies survive wasp attack when the fly carries protective bacteria, allowing us to experimentally test whether protection facilitates symbiont transfer from wasp to fly. Problem 2: What determines whether symbioses are stable? When symbionts transfer into a new host species, the symbioses are commonly unstable; the microbes often show weak transmission and may be lost in response to environmental stress. We do not currently understand why symbiotic stability varies. We hypothesise that symbiosis instability arises when dormant viruses (prophage) carried in the symbiont become activated, killing the symbiont. We will test this novel hypothesis using symbionts of aphids, ladybirds and flies. These symbionts carry dormant prophage and can be artificially transferred to new hosts easily. We know these transfers have varying stability, and that stability is affected by thermal environment. Applications and benefits. This project examines fundamental processes underpinning biodiversity, namely the commonness of biologically and ecologically crucial partners of arthropods. Our work seeks to explain why symbionts are so common, how existing symbionts shape the spread of others, why particular host species are infected, and how symbioses will respond to environmental change. This project also underpins application. Symbionts are transferred into pest and vector species to reduce the harm these insect cause, but symbiosis instability commonly prevents use. If our hypotheses are correct, they open new strategies to strengthen symbiosis stability and broaden application for human health and agricultural benefit.