Geographic Variation in Social Parasite Pressure Predicts Intraspecific but not Interspecific Aggressive Responses in Hosts of a Slavemaking Ant

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.

The ecological success of a social parasite increases with manipulation of collective host behaviour

“…Moreover, T. curvispinosus colonies were more aggressive towards a live slavemaker than T. longispinosus ( z = −3.18, P = 0.001; also shown in Jongepier et al ., ). This difference was not driven by species‐specific variation in aggressive potential towards slavemakers, as T. longispinosus colonies were more, not less aggressive towards a dead slavemaker ( z = 4.41, P < 0.0001; also shown in Kleeberg et al ., ).…”

“…In addition, we recorded whether the colony evacuated its nest site within six hours of slavemaker introduction and whether the slavemaker managed to escape, physically unharmed and therefore able to recruit nestmates and initiate a slave raid. To control for differences in aggressive potential between colonies, we further included data on colony aggression towards a dead slavemaker, previously published in Kleeberg et al . (). Hereto, we introduced a freshly frozen slavemaker worker and recorded the number of aggressive workers (i.e.…”

“…Nonetheless, standardization could potentially cause confounding effects due to local adaptation in the two populations that were tested against a sympatric slavemaker, or the lack thereof in the remaining 14 populations. Several studies, however, found no evidence that Temnothorax hosts are better adapted to their local slavemaker (Foitzik et al ., ; Brandt & Foitzik, ), which included tests of local host adaptation in aggression towards live and dead slavemakers (Jongepier et al ., ; Kleeberg et al ., ). Although we did not test for local host adaptation in the hosts’ Dufour‐treated nestmate attack, we could show that the exclusion of populations tested against a sympatric slavemaker did not qualitatively change the outcome of our analyses, nor were the hosts’ aggressive responses related to the geographic distance between the Temnothorax population and the slavemaker population of origin (Dufour‐treated nestmate attack: t 14 = 0.51, P = 0.615; aggression towards a live parasite: t 14 = −0.45, P = 0.662).…”

“…This decrease in host aggression with slavemaker prevalence was not due to geographic variation in the aggressive potential of Temnothorax colonies (i.e. aggression in the absence of manipulation; Kleeberg et al ., ). Hence, we hypothesize that populations that are better defended against slavemakers are more resistant to manipulation of their aggressive responses, resulting in lower slavemaker prevalence in the field.…”

The placid slavemaker: avoiding detection and conflict as an alternative, peaceful raiding strategy

“…These raids often escalate into violent fights, as hosts fiercely defend their young. Slavemaking ants can show high prevalence, so that the resulting parasite pressure can lead to the evolution of fine-tuned host defense strategies, including enemy recognition, flight, and fighting strategies Bauer et al 2009;Jongepier et al 2014;Kleeberg et al 2014Kleeberg et al , 2015. These host defenses might be one of the reasons why slavemakers generally do not employ a sneaking strategy or avoid aggressive escalations during raids.…”