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.

Keywords: brood parasites; defence portfolios; frontline defences; host–parasite interaction; social insects.

Figure 1.

Distribution of experimental Temnothorax host populations and parasite pressure by the slavemaker ant P. americanus. Pie diagrams and numbers represent parasite prevalence and median slavemaker colony sizes (i.e. the median number of slavemaker workers), respectively, in Illinois (IL), Indiana (IN), Kentucky (KY), Maine (ME), Massachusetts (MA), New Hampshire (NH), New Jersey (NJ), New York (NY), Ohio North (OHn), Ohio South (OHs), Quebec (QC), Vermont (VT), Virginia (VA) and West Virginia (WV). Details on collection sites are provided in the electronic supplementary material.

Figure 2.

Collective host defences in relation to social parasite pressure. Parasite pressure is represented by the parasite prevalence (a,c) and the median slavemaker colony size (b,d). Symbols represent the estimate ± s.e. per population, standardized for average host colony size (i.e. population estimates + colony size estimate × average host colony size). Regression lines are derived from the following GLMM estimates and back-transformed to the original data scale. (a) Estimate ± s.e. = −3.77 ± 1.31, z = −2.89, p = 0.004; (b) −0.25 ± 0.07, z = −3.49, p < 0.001; (c) 6.84 ± 2.40, z = 2.85, p = 0.004 and (d) 0.42 ± 0.14, z = 3.02, p = 0.003.

Figure 3.

Differences in aggressive defence strategies and efficiency between host species. Symbols represent the GLMM estimates ± s.e. (a) z = −5.45, p < 0.0001; (b) z = 4.54, p < 0.0001; (c) z = 5.30, p < 0.0001.