Collaborative Research: Competition and cooperation in the defensive symbiont communities of aphids

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Insects comprise the bulk of animal diversity on the planet and are often infected with microbes called 'symbionts'. Microbial symbionts can have large effects on their host insects, shaping their interactions with other species or their responses to the non-living environment. This is especially well-studied for plant sap-feeding insects, known as aphids, which can carry various combinations of over ten maternally transferred symbiont species. These symbionts influence aphids' interactions with food plants, protect aphids from attack by parasites and pathogens, or alleviate the effects of temperature changes. Since insects are important vectors of human disease and major agricultural pests, understanding the roles of these 'hidden players', and the mechanisms underlying symbiont function is important to further human interests in crop protection and preventing disease spread. Most studies to date have investigated the effects of single symbiont species infections, even though most insects carry multi-species symbiont 'communities'. This award will use a highly-tractable aphid model system, with well-characterized bacterial symbionts, to identify the effects of competition and cooperation amongst multiple symbionts on symbiont transmission, localization and aphid biology. Researchers will use newly developed culturing methods combined with genomic and gene expression studies, to investigate how these effects are generated. Since maternally transferred symbionts are widespread in insects, findings from the aphid model are relevant to crop and medical pests. In addition, this award supports the training and professional development of high school, undergraduate, graduate and post-doctoral researchers, and includes outreach events into the communities of the investigators. The pea aphid, Acyrthosiphon pisum, harbors a diverse cohort of facultative, maternally transferred symbionts and is an important model for defensive symbiosis. Recent field-based research shows that most individual pea aphids, with a facultative symbiont, harbor two or more species. Interestingly, symbiont distributions are non-random, with enriched co-infection among some symbiont pairs and rare co-infection among others, leading to the prediction that natural selection favors co-infections between symbionts with distinct defensive roles, establishing 'generalist' aphids protected against multiple threats. However, just a subset of such partnerships is likely favored as pairings between rare symbiont partners could heighten costs or emergent pathogenicity. Alternatively, rarity of some co-infections may stem from within-host symbiont interactions, including competition and resulting decreases in transmission rates. Conversely, common co-infections may stem from non-competing, cooperative symbionts that reciprocally enhance transmission. This award will test these different scenarios through manipulative experiments on engineered aphid lines that measure the impacts of co-infection context on symbiont-mediated protective phenotypes and rates of symbiont transfer. Symbiont densities and localization will be linked to aphid fitness, defensive phenotypes, symbiont interactions, and rates of transmission. In addition, genomic and gene-expression analyses of symbionts will be used to identify mechanisms underlying competitive and cooperative dynamics that are predicted to structure pea aphids' symbiont 'communities'. This research will enhance the understanding of multipartite symbioses in insect pests, with implications for mitigating their damage to human health, livestock, agriculture, and infrastructure. It will provide training to high school, undergraduate, graduate and postdoctoral students and enhance outreach to the local community.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.