Collective defence portfolios of ant hosts shift with social parasite pressure

Abstract

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.

Latitudinal variation in behaviors linked to risk tolerance is driven by nest-site competition and spatial distribution in the ant Temnothorax rugatulus

“…Indeed, stickleback populations show differential patterns and consistency of risk tolerance between populations with and without predators (Bell and Stamps 2004). Similarly, social parasitism, where one social group benefits at the expense of another, has been shown to affect colony defensive behavior in Temnothorax ants (Pamminger et al 2012;Jongepier et al 2014), though such social parasitism has not been investigated in T. rugatulus. A second hypothesis is that competition for resources may drive the level of risk tolerance (Grand and Dill 1999).…”

The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons

“…Just as Polyergus queens change their chemical strategies from insignificance to camouflage [64], T. pilagens might adapt its profile during the raiding season. The lack of mimicry in slavemakers may be owing to host defences [40,65,66]: the host T. longispinosus has evolved counter-adaptations [47,65,67], including chemical profile diversification, preventing the parasite from matching all host colonies [26]. With few exceptions [58], chemical mimicry allows adaptation only to a single host.…”

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.…”

“…Next to aggression as a beneficial anti-parasite defense (Pamminger et al 2012;Kleeberg et al 2014), host colonies also react with fast nest evacuation (Alloway 1979;Jongepier et al 2014). Slavemakers try to undermine these adaptive host responses through behavioral (e.g., nest entrance guarding; Alloway 1979) or chemical strategies, such as manipulation through the use of the Dufour's gland Brandt et al 2006).…”