Symbiont-assisted cuticle biosynthesis as a key innovation contributing to the evolutionary success of beetles

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To elucidate the key adaptations underlying evolutionary success remains one of the central challenges in evolution and ecology. However, rigorous experimental tests are usually hampered by the lack of replicate evolutionary events or the inability to manipulate a candidate trait of importance. SYMBeetle exploits the naturally replicated evolution of an experimentally tractable, symbiont-assisted key adaptation in beetles to understand its impact on niche expansion and diversification. Recent evidence indicates that beetles across at least seven different families associate with microbial symbionts that provision their host with tyrosine, an aromatic amino acid necessary for cuticle biosynthesis, hardening, and tanning. SYMBeetle addresses the hypothesis that the acquisition of tyrosine-supplementing microbes constituted a key innovation across phylogenetically distinct beetles that allowed them to expand into novel ecological niches, by relaxing the dependence on nitrogen-rich diets for successful formation of the rigid exoskeleton and protective front wings. Specifically, tyrosine supplementation may facilitate the transition to herbivory and allow for subsisting at very low ambient humidity, by facilitating the production of a thick cuticular barrier to desiccation. To test this, SYMBeetle will uniquely combine experimental manipulation of symbiotic associations to assess the symbionts’ contribution to cuticle biosynthesis and its fitness consequences (desiccation resistance and defense) with large-scale comparative approaches aimed at elucidating the taxonomic distribution, ecological contexts, and evolutionary origins of cuticle-supplementing symbioses. The results are expected to transform our understanding of microbes as important facilitators for the evolution of herbivory and the colonization of dry habitats in beetles, two factors of major relevance for the emergence of economically relevant insect pests of agricultural crops and stored products.