Symbiosis and horizontal gene transfer promote herbivory in the megadiverse leaf beetles

Beetles that feed on the nutritionally depauperate and recalcitrant tissues provided by the leaves, stems, and roots of living plants comprise one-quarter of herbivorous insect species. Among the key adaptations for herbivory are plant cell wall-degrading enzymes (PCWDEs) that break down the fastidious polymers in the cell wall and grant access to the nutritious cell content. While largely absent from the non-herbivorous ancestors of beetles, such PCWDEs were occasionally acquired via horizontal gene transfer (HGT) or by the uptake of digestive symbionts. However, the macroevolutionary dynamics of PCWDEs and their impact on evolutionary transitions in herbivorous insects remained poorly understood. Through genomic and transcriptomic analyses of 74 leaf beetle species and 50 symbionts, we show that multiple independent events of microbe-to-beetle HGT and specialized symbioses drove convergent evolutionary innovations in approximately 21,000 and 13,500 leaf beetle species, respectively. Enzymatic assays indicate that these events significantly expanded the beetles’ digestive repertoires and thereby contributed to their adaptation and diversification. Our results exemplify how recurring HGT and symbiont acquisition catalyzed digestive and nutritional adaptations to herbivory and thereby contributed to the evolutionary success of a megadiverse insect taxon. [Display omitted] •Genomics and transcriptomics resolve the phylogeny of leaf beetle subfamilies•Plant cell wall-degrading enzymes (PCWDEs) show a dynamic evolutionary history•Multiple symbiont acquisitions and horizontal gene transfers contributed new PCWDEs•Symbiosis and HGT expanded beetles’ digestive repertoires, fueling their success Leaf beetles are among the most speciose herbivores on earth. Kirsch et al. show that multiple independent symbiont acquisitions and microbe-to-host horizontal gene transfers shaped the beetles’ repertoire of plant cell wall-degrading enzymes, catalyzing digestive adaptations and contributing to the evolutionary success of this megadiverse taxon.