Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance

The evolutionary interactions between permanently social parasitic species and their hosts are of special interest because social parasites are not only closely dependent on, but are also closely related to, their hosts. The small European slavemaker Harpagoxenus sublaevis has evolved several characters that help manipulate its host. In this study we investigated adaptations of this social parasite to its local hosts and the geographic pattern of host resistance in two main host species from three different populations. In behavioral experiments, we examined whether host colonies from three geographically distant Leptothorax acervorum populations varied in their ability to defend the nest against social parasites. Naive colonies from the unparasitized English population killed attacking slavemakers more often than did host colonies from two parasitized populations. We also found strong interpopulation variation in the ability of the slavemaker to manipulate host behavior. H. sublaevis uses the Dufour gland secretion to induce intracolonial fights and, in general, this propaganda substance was most effective against local hosts. Our results suggest that the social parasite is leading the arms race in this aspect. Similar experiments uncovered differences between two populations of the second host species L. muscorum and could demonstrate that nest defense in both host species is similarly efficient. In L. acervorum, monogynous colonies were more successful in nest defense, whereas social structure had no impact in L. muscorum. Colony size did not affect the efficacy of nest defense in either host species. The caste of the slavemaker had a strong influence on the success of an attack.