Symbiosis and horizontal gene transfer shaped the evolution of herbivory in leaf beetles
A third of all animal species are herbivorous, exploiting a diet rich in complex cell wall polysaccharides such as cellulose and pectin. While many herbivorous insects employ plant cell wall-degrading enzymes (PCWDEs) to access the nutritious cell content, a comprehensive overview on the diversity of enzymatic repertoires and their evolutionary dynamics remains lacking. Here, we illustrate that multiple events of microbe-to-beetle horizontal gene transfer (HGT) of PCWDEs as well as at least three independent acquisitions of nutritional symbionts shaped the evolution of plant cell wall digestion in leaf beetles - one of the most speciose lineages of herbivorous animals on earth. Genomic and transcriptomic analyses of 74 hosts and 50 symbionts across all recognized leaf beetle subfamilies as well as enzymatic assays illustrate the dynamic evolutionary history of PCWDEs and reveal that HGT and symbiosis resulted in convergent evolutionary innovations in an estimated 21,000 and 13,500 species of leaf beetles, respectively. Our results exemplify how HGT and symbiont acquisition catalyzed digestive and nutritional adaptations to herbivory and thereby contributed to the evolutionary success of a megadiverse insect taxon.