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.

No abstract

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.

Host entry is a crucial step in a parasite's life cycle. When parasites manage to circumvent host detection, exploitation of host resources is facilitated, as host defenses have not to be counteracted. Social parasites exploit animal societies and, likewise, detection avoidance can be beneficial. Yet, due to strong selection pressures, hosts of socially parasitic slavemaking ants often recognize them as enemies, so that slavemakers use open force to raid host colonies. These fights, however, prohibit the enslavement of adult host workers (eudulosis), which cannot be manipulated to work for them. Instead, they steal brood during raids, and enslave those upon emergence. In contrast to the violent raids of most slavemakers, no aggression occurs during most of the raids of the newly described slavemaker Temnothorax pilagens. Thereby, T. pilagens regularly induces adult host workers to be part of their slave workforce. We demonstrate that nonenslaved colonies of its host species respond to this slavemaker with little aggression. We further investigate how the slavemaker circumvents recognition and show that chemical resemblance of host profiles might explain the low aggressive responses. But, which parameters determine whether slave raids escalate, resulting in carnage among defenders? Our experiments reveal that host aggression is counterproductive as aggressive host colonies suffer from more fatalities during raids, but cannot save more brood. The slavemaker, however, benefits from not eliciting fights, as it doubles its enslaved workforce by capturing brood plus adult host workers. Hence, undercutting recognition allows the slavemaker to avoid raid escalation with its associated fitness benefits.

Chemical communication is central for the formation and maintenance of insect societies. Generally, social insects only allow nest-mates into their colony, which are recognized by their cuticular hydrocarbons (CHCs). Social parasites, which exploit insect societies, are selected to circumvent host recognition. Here, we studied whether chemical strategies to reduce recognition evolved convergently in slavemaking ants, and whether they extend to workers, queens and males alike. We studied CHCs of three social parasites and their related hosts to investigate whether the parasitic lifestyle selects for specific chemical traits that reduce host recognition. Slavemaker profiles were characterized by shorter-chained hydrocarbons and a shift from methyl-branched alkanes to n -alkanes, presumably to reduce recognition cue quantity. These shifts were consistent across independent origins of slavery and were found in isolated ants and those emerging in their mother colony. Lifestyle influenced profiles of workers most profoundly, with little effect on virgin queen profiles. We detected an across-species caste signal, with workers, for which nest-mate recognition is particularly important, carrying more and longer-chained hydrocarbons and males exhibiting a larger fraction of n -alkanes. This comprehensive study of CHCs across castes and species reveals how lifestyle-specific selection can result in convergent evolution of chemical phenotypes.