Origin and function of beneficial bacterial symbioses in insects

Beneficial bacterial symbionts are widespread in insects and affect the fitness of their hosts by contributing to nutrition, digestion, detoxification, communication or protection from abiotic stressors or natural enemies. Decades of research have formed our understanding of the identity, localization and functional benefits of insect symbionts, and the increasing availability of genome sequences spanning a diversity of pathogens and beneficial bacteria now enables comparative approaches of their metabolic features and their phylogenetic affiliations, shedding new light on the origin and function of beneficial symbioses in insects. In this Review, we explore the symbionts’ metabolic traits that can provide benefits to insect hosts and discuss the evolutionary paths to the formation of host-beneficial symbiotic associations. Phylogenetic analyses and molecular studies reveal that extracellular symbioses colonizing cuticular organs or the digestive tract evolved from a broad diversity of bacterial partners, whereas intracellular beneficial symbionts appear to be restricted to a limited number of lineages within the Gram-negative bacteria and probably originated from parasitic ancestors. To unravel the general principles underlying host–symbiont interactions and recapitulate the early evolutionary steps leading towards beneficial symbioses, future efforts should aim to establish more symbiotic systems that are amenable to genetic manipulation and experimental evolution.