Coevolution in host–parasite systems: behavioural strategies of slave–making ants and their hosts

Abstract

Recently, avian brood parasites and their hosts have emerged as model systems for the study of hostp arasite coevolution. However, empirical studies of the highly analogous social parasites, which use the workers of another eusocial species to raise their own young, have never explicitly examined the dynamics of these systems from a coevolutionary perspective. Here, we demonstrate interpopulational variation in behavioural interactions between a socially parasitic slave-maker ant and its host that is consistent with the expectations of host^parasite coevolution. Parasite pressure, as inferred by the size, abundance and raiding frequency of Protomognathus americanus colonies, was highest in a New York population of the host Leptothorax longispinosus and lowest in a West Virginia population. As host^parasite coevolutionary theory would predict, we found that the slave-makers and the hosts from New York were more e¡ective at raiding and defending against raiders, respectively, than were conspeci¢cs from the West Virginia population. Some of these variations in e¤cacy were brought about by apparently simple shifts in behaviour. These results demonstrate that defence mechanisms against social parasites can evolve, and they give the ¢rst indications of the existence of a coevolutionary arms race between a social parasite and its host.

Collective defence portfolios of ant hosts shift with social parasite pressure

“…Nonetheless, hosts of insect social parasites and avian brood parasites show striking similarities in the trajectories and outcomes of their coevolutionary arms races [3]. Like avian hosts, social insects exhibit a range of morphological, behavioural and physiological adaptations to social parasites, which often co-occur in a single host species [9][10][11][12][13]. The apparent depth of these defence portfolios renders social parasitic hosts particularly suitable targets in the study of host defence portfolios [3].…”

Geographic distribution of the anti-parasite trait “slave rebellion”

“…It is not easy to quantify parasite pressure, because it depends on several parameters such as parasite prevalence, raid frequency and destructiveness as well as community composition. Previous studies have shown that parasite prevalence is very similar in the three focal communities (Table 1), but slavemaker colonies in NY seem to have a higher frequency of successful raids as compared to WV and OH (Foitzik et al 2001, Brandt & Foitzik 2004). …”

“…This suggests that the slavemaker might lead the arms race in NY, for example, by closely tracking host pupae profiles. In addition, it is possible that a higher number of raided host nests survive in WV, where slavemaker are less destructive during raids (Foitzik et al 2001). If so, slaves in WV might be more likely to have nests with relatives in the vicinity.…”

“…Most studies have focused on adaptations prior to enslavement including enemy recognition, adjustment of the recognition threshold, fighting abilities, inducible aggression and fast evacuation and escape from the attacked host colonies (Alloway 1990;Foitzik et al 2001;Brandt et al 2005Scharf et al 2011). …”

Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature

“…Counter-measures are therefore expected to be selected, as recently shown by Foitzik et al (2001) studying three populations of the pair Protomognathus americanus/Leptothorax longispinosus. As a consequence of higher parasite pressure, the host population becomes more effective in defending against raiders.…”