Increased genetic diversity as a defence against parasites is undermined by social parasites: Microdon mutabilis hoverflies infesting Formica lemani ant colonies.

Genetic diversity can benefit social insects by providing variability in immune defences against parasites and pathogens. However, social parasites of ants infest colonies and not individuals, and for them a different relationship between genetic diversity and resistance may exist. Here, we investigate the genetic variation, assessed using up to 12 microsatellite loci, of workers in 91 Formica lemani colonies in relation to their infestation by the specialist social parasite Microdon mutabilis. At the main study site, workers in infested colonies exhibited lower relatedness and higher estimated queen numbers, on average, than uninfested ones. Additionally, estimated queen numbers were negatively correlated with estimated average numbers of mates per queen within infested colonies. At another site, infested colonies also exhibited significantly lower worker relatedness, and estimated queen numbers were comparable in trend. In contrast, in two populations of F. lemani where M. mutabilis was absent, relatedness within colonies was high (40 and 90% with R>0.6). While high genetic variation can benefit social insects by increasing their resistance to pathogens, there may be a cost in the increased likelihood of infiltration by social parasites owing to greater variation in nestmate recognition cues. This study provides the first empirical test of this hypothesis.