Evolution, ecology, and molecular regulation of tyrosine-supplementing symbioses in beetles

The insect cuticle represents an important barrier against desiccation and natural enemies. For the biosynthesis of the cuticular proteins, the cross-linking with chitin, and the coloration via melanin, insects require high amounts of the semi-essential aromatic amino acid tyrosine during metamorphosis. This is especially true for beetles, because of their particularly strong body armor and the heavily sclerotized front wings (elytra). Like other animals, however, beetles are unable to synthesize tyrosine, and the acquisition of sufficient amounts of tyrosine from dietary sources can be challenging, particularly for herbivorous taxa. Here we show that symbiotic microbes represent a widespread and ecologically important alternative source of tyrosine, with at least seven independent evolutionary origins in herbivorous beetles. While each association shows its own evolutionary dynamics, all converged on intracellular bacteriome-localized symbioses with severely genome-eroded bacterial partners, streamlined for the biosynthesis of tyrosine via the shikimate pathway. Experimental manipulation of the symbiosis in the silvanid beetle Oryzaephilus surinamensis demonstrates that the symbiont-mediated tyrosine provisioning contributes to cuticle thickness, hardening, and tanning. Consequently, symbiotic beetles are better protected from desiccation, predator and pathogen attack, but in turn also become susceptible to the widely used herbicide glyphosate that targets the shikimate pathway. Gene expression profiling and targeted knock-down of candidate genes yield insights into the metabolic cross-talk and molecular regulation of the symbiosis. Our results reveal tyrosine limitation as a widespread and as yet underestimated challenge for herbivorous insects, and show that tyrosine-supplementing intracellular symbioses are widespread and ecologically important in beetles.