Locally adapted social parasite affects density, social structure, and life history of its ant hosts.

Selection and adaptation are important processes in the coevolution between parasites and their hosts. The slave-making ant Protomognathus americanus, an obligate ant social parasite, has previously been shown to evolve morphological, behavioral, and chemical adaptations in the coevolutionary arms race with its Temnothorax hosts. Yet empirical studies have given variable results on the strength of the selection pressure this parasite exerts on its host populations. In this study, we directly investigated the pressure exerted by P. americanus and the reactions of the main host species, T. longispinosus, in two ant communities by manipulating parasite density in the field over several years. In addition, a cross-fostering design with the exchange of parasites between host populations allowed us to investigate local adaptation of parasite or host. We demonstrate a severe impact of the social parasite on the two host populations in West Virginia and New York, but also variation in host reactions between sites, as expected by the geographic mosaic theory of coevolution. Host density decreased at the West Virginia site with the presence of local slave-makers, whereas at the ecologically favorable New York site, density was unaffected. Nevertheless, social organization, colony size, and investment patterns of these host colonies at this site changed in response to our parasite manipulation. The release of P. americanus colonies led to a reduction in the number of resident queens and workers, an increase in intranest relatedness, and lower productivity, but also a higher investment in reproductives. In West Virginia, colony demography did not change, but raiding activity by New York slave-makers caused different investment patterns of host colonies. In addition, the cross-fostering element revealed local adaptation of the parasite P. americanus: slave-making colonies fared better in their sympatric host population, as they contained more slave-making ant workers and slaves at the end of our 27-month experiment.