Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host's nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.

Variation in community composition over a species' geographic range leads to divergent selection pressures, resulting in interpopulation variation in trait expression. One of the most pervasive selective forces stems from antagonists such as parasites. Whereas hosts of microparasites developed sophisticated immune systems, social parasites select for behavioural host defences. Here, we investigated the link between parasite pressure exerted by the socially parasitic slavemaking ant Protomognathus americanus and colony-level aggression in Temnothorax ants from 17 populations. We studied almost the entire geographic range of two host species, including unparasitized populations. As previous studies have demonstrated that host colonies responding highly aggressively towards conspecifics fare better during slavemaker attacks, we predicted higher aggression levels in severely parasitized populations. Indeed, we demonstrate an increase in aggression towards conspecifics with parasite pressure, a pattern that was consistent over the two host species. In contrast to other studies, aggression against the parasite itself did not shift with parasite pressure. This may be explained by an absence of costs of parasite-specific aggression in parasite-free populations. The preferred host species T. longispinosus was generally more aggressive; however, the association between parasite pressure and aggression was found for both species, suggesting convergent co-adaptation. Two potentially confounding factors, colony density and the co-occurrence of a competing Temnothorax species in the community, could not explain the level of colony aggression in intra-and interspecific interactions. Instead, our study points to social parasite pressure as the determining factor shaping antagonistic interactions within, but not between, host species.