Local adaptation to hosts and parasitoids shape Hamiltonella defensa genotypes across aphid species

Facultative symbionts are common in insects and can provide their hosts with significant adaptations. Yet we still have a limited understanding of what shapes their distributions, such as why particular symbiont strains are common in some host species yet absent in others. To address this question, we genotyped the defensive symbiont Hamiltonella defensa in 26 aphid species that commonly carry this microbe. We found that Hamiltonella strains were strongly associated with specific aphid species and that strains found in one host species rarely occurred in others. To explain these associations, we reciprocally transferred the Hamiltonella strains of three aphid species, Acyrthosiphon pisum, Macrosiphoniella artemisiae and Macrosiphum euphorbiae, and assessed the impact of Hamiltonella strain on: the stability of the symbiosis, aphid fecundity and parasitoid resistance. We demonstrate that the Hamiltonella strains found in nature are locally adapted to specific aphid hosts, and their ecology: aphids tend to carry Hamiltonella strains that are efficiently transmitted to their offspring, non-lethal, and that provide strong protection against their dominant parasitoid species. Our results suggest that facultative symbiont distributions are shaped by selection from natural enemies, and the host itself, resulting in locally adapted symbioses that provide significant benefits against prevailing natural enemies.