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 to their degree of behavioural integration into the colony and to their accuracy of chemically imitating 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 to 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.
1. A diverse group of arthropods have adapted to the niches found inside the nests of social insects. Studies mostly focused on very specialised parasites residing in the brood chambers. However, the biology and strategies of symbionts occupying other niches, such as waste dumps, are underexplored.2. Using a series of complementary experiments, this study demonstrated that the Mediterranean beetle Oochrotus unicolor has adapted to the waste dump niche found in the nests of Messor harvester ants.3. Laboratory experiments confirmed field observations that the beetle preferentially resided in the refuse pits. Next, it was shown that the beetles readily consumed seeds and flour, whereas other food sources were poorly accepted and ant brood was never even eaten. The beetles did not elicit a strong aggression response in Messor ants, and they could tolerate very high densities of workers without clear costs. The beetles modestly mimicked the nest recognition cues of their Messor host. This imperfect mimicry could promote the adoption of the beetle in the ant colony, in concert with mechanical defence generated by its tank-like body. Isolation of the beetle from its host did not significantly affect the beetle's chemical cuticular profile nor did it provoke elevated ant aggression, indicating that the beetle does not acquire the chemicals passively from its host.4. This paper discusses the fact that waste dumps in social insect nests are hotspots for arthropod symbionts. It shows that symbionts in this niche may employ behavioural, trophic and chemical strategies that are different from those found in other niches of social insect nests.
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