Adaptation and diversification of tortoise beetles in light of symbiont metabolic variation

• Applicant: Dr. Hassan Salem
• Subject Area: Animal Physiology and Biochemistry ; Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
• Term: since 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 513349254

Microbial symbionts are a key source of evolutionary innovation in insects. By upgrading host metabolism and physiology, beneficial microbes can promote insect adaptation and facilitate the expansion into novel ecological space. While obligate symbionts are generally prevalent across the insect tree of life, they are especially common among herbivorous clades. Our prior work on tortoise leaf beetles (Coleoptera: Chrysomelidae: Cassidinae) revealed that the γ- proteobacterial symbiont, Stammera, is essential for host development and survival. Stammera possesses a drastically reduced genome that is streamlined for the production and export of pectinases, enabling its host to digest foliage rich in recalcitrant pectins. Despite a high degree of genomic conservation, Stammera varies across host species in the pectinases it encodes and supplements. While all Stammera strains encode polygalacturonase, a subset of species additionally supplement rhamnogalacturonan lyase. As Cassidinae beetles symbiotically endowed with both pectinases exhibit a wider distribution and exploit a greater variety of host-plants, this proposal aims to characterize the causal link between a symbiont’s metabolic potential and the ecological radiation of its host. The proposal features two projects. The first will address the adaptive importance and ecological relevance of Stammera-encoded rhamnogalacturonan lyase to tortoise beetles. Using a combination of manipulative bioassays, biochemical characterizations, and immunohistochemistry, we will characterize how rhamnogalacturonan lyase shapes host digestive physiology and affects development and fitness. The second project will examine the impact of an expanded symbiont digestive range on host beetle diversification. As symbiont- encoded rhamnogalacturonan lyase expands the availability of ecologically accessible resources to a subset of Cassidinae species – corresponding to a broader ecological range – this project asks whether niche expansion is concomitant with elevated diversification rates. Metagenomic data will be generated for beetle species across all 43 tribes within the Cassidinae subfamily and spanning a representative range of ecological guilds. On the symbiont side, the generated genomic data will conclusively define the Stammera pangenome, its core genes, and the accessory pathways that reflect differences in host ecology. On the host side, a phylogeny is intended to resolve Cassidinae relationships at the tribe-level and estimate host diversification rates. Importantly, both efforts should shed light on when rhamnogalacturonan lyase was acquired by Stammera, and how that acquisition impacted the diversification of its Cassidinae hosts. Collectively, the proposed research should contribute to our general understanding of animal-microbe interactions by shedding light on how variation in symbiont metabolic potential can differentially and fundamentally shape host adaptation, distribution, and diversification.

• DFG Programme: Research Grants