Polyandry and paternity affect disease resistance in eusocial wasps: support for the parasite–pathogen hypothesis

Abstract

Polyandry (multiple mating by females) is a central challenge for understanding the evolution of eusociality. Several hypotheses have been proposed to explain its observed benefits in eusocial Hymenoptera, and one, the parasite-pathogen hypothesis, proposes that high genotypic variance among workers for disease resistance prevents catastrophic colony collapse. We tested the parasite-pathogen hypothesis in the polyandrous wasp Vespula shidai. We infected isolated workers with the entomopathogenic fungus Beauveria bassiana and quantified their survival in the laboratory. Additionally, we conducted paternity analysis of the workers using nine microsatellite loci to investigate the relationship between survival and matriline/patriline of the workers. As predicted by the parasite-pathogen hypothesis, nestmate workers of different patrilines showed differential resistance to B. bassiana. We also demonstrated variations in virulence among strains of B. bassiana. Our results are the first to directly support the parasitepathogen hypothesis in eusocial wasps and suggest that similar evolutionary pressures drove the convergent origin and maintenance of polyandry in ants, bees, and wasps.