The transition to a social parasitic lifestyle influences maintenance and expression of essential immune defence traits

Abstract Social parasites and their equally social hosts offer interesting systems to understand gains and losses in evolution. Yet, they have so far rarely been used to study the evolution of immune defence traits. To gain a better understanding of the evolutionary consequences of a transition to a social parasitic lifestyle on immune defence traits, here we investigated the facultative social parasitic ant Formica sanguinea , the obligate social parasitic ant Polyergus rufescens and their common social host ant species Formica fusca in mixed as well as single species experimental setups. We found that during sanitary care of fungal entomopathogen exposed pupae, F. fusca performs not only most of the sanitary behaviour of brood grooming but performs brood grooming also according to the degree of social parasite specialization, engaging in four and ten times more brood grooming in mixed setups involving F. sanguinea and P. rufescens , respectively. We also found that F. sanguinea engages in brood grooming and worker allo-grooming irrespective of F. fusca presence, while P. rufescens never expressed these sanitary behaviours. Consequently, the presence of F. fusca delayed fungal outgrowth on brood of P. rufescence and diminished its worker mortality risk, while F. fusca presence was not similarly beneficial to F. sanguinea . Finally, we found that in the absence of F. fusca , F. sanguinea upregulates the use of venom for sanitary purposes. We conclude that social parasites are interesting systems to study the maintenance and expression of immune defence traits and the evolutionary pressures that shape investment in these traits. Significance statement The transition to a social parasitic lifestyle may alleviate selective pressures at maintaining or expressing immune defence traits that are essential for free-living species, with social parasites instead relying on immune services provided by their social host. We explored this in two dulotic (aka “slave-making”) social parasites that differ in the degree of their dependence on the parasitic mode of life and their common host species during sanitary care of fungus-infected brood. We found that the host showed increased brood grooming rates towards social parasitic brood indicating exploitation of social immune services. We also found that the facultative social parasite has retained immune defence traits, likely to be able to survive without a host, while the obligate social parasite relies on immune services provided by the host and has lost essential immune defence traits, like many other ancestral traits associated with a free-living cooperative life style.