Chemical and Behavioural Strategies along The Spectrum of Host Specificity in Ant-Associated Silverfish

Background Host range is a fundamental trait to understand the ecological and evolutionary dynamics of symbionts. Increasing host specificity is expected to be accompanied with specialization in different symbiont traits. We tested this specificity-specialization association in a large group of 16 ant-associated silverfish species by linking their level of host specificity with their degree of behavioural integration into the colony and their accuracy of chemically deceiving the host’s recognition system, i.e. the cuticular hydrocarbon (CHC) profile. Results As expected, facultative associates and host generalists (targeting multiple unrelated ants) tend to avoid the host, whereas host-specialists (typically restricted to Messor ants) were bolder, approached the host and allowed inspection. Generalists and host specialists regularly followed a host worker, unlike the other silverfish. Host aggression was extremely high toward non-ant-associated silverfish and modest to low in ant-associated groups. Surprisingly, the degree of chemical deception was not linked with host specificity as most silverfish, including facultative ant associates, imitated the host’s CHC profile. Messor specialists retained the same CHC profile as the host after moulting, in contrast to a host generalist, suggesting an active production of the cues (chemical mimicry). Host generalist and facultative associates flexibly copied the highly different CHC profiles of alternative host species, pointing at passive acquisition (chemical camouflage) of the host’s odour. Conclusions Overall, we found that behaviour that seems to facilitate the integration in the host colony was more pronounced in host specialist silverfish. Chemical deception, however, was employed by all ant-associated species, irrespective of their degree of host specificity.

The possible role of ant larvae in the defence against social parasites

Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca , consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.