Do well-integrated species of an inquiline community have a lower brood predation tendency? A test using red wood ant myrmecophiles

Thomas Parmentier, Wouter Dekoninck, Tom Wenseleers

A host infected with multiple parasitic species provides a unique system to test evolutionary and ecological hypotheses. Different parasitic species associated with a single host are expected to occupy different niches. This niche specialization can evolve from intraguild competition among parasites. However, niche specialization can also be structured directly by the host when its defence strategy depends on the parasite's potential impact. Then it can be expected that species with low or no tendency to prey on host brood will elicit less aggression than severe brood parasitic species and will be able to integrate better in the host system. We examined this hypothesis in a large community of symbionts associated with European red wood ants (Formica rufa group) by testing the association between 1) level of symbiont integration (i.e. presence in dense brood chambers vs. less populated chambers without brood) 2) level of ant aggression towards the symbiont 3) brood predation tendency of the symbiont. Symbionts differed vastly in integration level and we demonstrated for the first time that relatively unspecialized ant symbionts or myrmecophiles occur preferentially in brood chambers. Based on their integration level, we categorize the tested myrmecophiles into three categories: 1) species attracted to the dense brood chambers 2) species rarely or never present in the brood chambers 3) species randomly distributed throughout the nest. The associates varied greatly in brood predation tendency and in aggression elicited. However, we did not find a correlation for the whole myrmecophile community between a) brood predation tendency and host's aggression b) integration level and host's aggression c) integration level and brood predation tendency. Our results indicate that red wood ants did not act more hostile towards species that have a high tendency to prey on brood compared to species that are less likely or do not prey on brood. We show that potentially harmful parasites can penetrate into the deepest parts of a social insect fortress. We discuss these seemingly paradoxical findings in relation to models on coevolution and evolutionary arms races and list factors which can make the presence of potentially harmful parasites within the brood chambers evolutionary stable.