Impact of parasite sympatry on the geographic mosaic of coevolution

Slave-making ants are specialized social parasites that steal the young from colonies of their host species to augment their slave supply. The degree of parasite-host specialization has been shown to shape the trajectory along which parasites and hosts coevolve and is a prime contributor to the geographic mosaic of coevolution. However, virtually nothing is known about extrinsic influences on parasite-host dynamics, although the simple addition of a competing slave-maker may significantly alter selection pressures. Here we report the effect of two sympatric slave-makers on a single host. We measured temporal and spatial changes in colonies of the primary host Temnothorax curvispinosus that had been placed in field enclosures along with a single colony of either one or both species of the North American slave-making ants Protomognathus americanus and Temnothorax duloticus. Each slave-maker species alone had a negative impact on its hosts, although one slave-maker species more frequently decimated its host assemblage and then went extinct. Nevertheless, the combined effect in mixed-parasite enclosures was, surprisingly, greatly attenuated. Virulent slave-maker growth and prudent slave-maker decay in these shared enclosures, together with field data showing an inverse proportional relationship between the two slave-makers in natural populations, suggest that their checkered distribution is a consequence of direct asymmetrical antagonism between parasites. Thus, our results imply a tripartite coevolutionary arms race, whereby intraguild interactions among social parasites strongly affect the realized selection pressures on hosts and contribute to the geographic mosaic of coevolution.