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Evolutionary stability of antibiotic protection in a defensive symbiosis

Significance Insights from natural applications of antibiotics are important to gain a deeper understanding of the evolutionary processes that underlie the maintenance of an antibiotic defense and prevent the rise and spread of antibiotic resistance. Using 25 species and subspecies of beewolf digger wasps that engage in a defensive symbiosis with Streptomyces bacteria, we tracked evolutionary changes in the antibiotic cocktail that protects the wasps’ larval offspring against mold fungi. Our results yield insights into the mechanistic basis as well as the ecological and evolutionary implications of producing a complex cocktail of antimicrobial compounds in a symbiotic setting. The increasing resistance of human pathogens severely limits the efficacy of antibiotics in medicine, yet many animals, including solitary beewolf wasps, successfully engage in defensive alliances with antibiotic-producing bacteria for millions of years. Here, we report on the in situ production of 49 derivatives belonging to three antibiotic compound classes (45 piericidin derivatives, 3 streptochlorin derivatives, and nigericin) by the symbionts of 25 beewolf host species and subspecies, spanning 68 million years of evolution. Despite a high degree of qualitative stability in the antibiotic mixture, we found consistent quantitative differences between species and across geographic localities, presumably reflecting adaptations to combat local pathogen communities. Antimicrobial bioassays with the three main components and in silico predictions based on the structure and specificity in polyketide synthase domains of the piericidin biosynthesis gene cluster yield insights into the mechanistic basis and ecoevolutionary implications of producing a complex mixture of antimicrobial compounds in a natural setting.