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

Abstract

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.

Co-habiting ants and silverfish display a converging feeding ecology

“…Atelura formicaria is known to steal food droplets from ant workers (Janet, 1897). However, these species are less inclined to approach the host compared to host-specialized silverfish (Parmentier et al, 2022). (4) Facultative generalist: this category includes Lepisma baetica (Lepismatidae) that occurs in ant nests, but can also be found away from ants.…”

“…(4) Facultative generalist: this category includes Lepisma baetica (Lepismatidae) that occurs in ant nests, but can also be found away from ants. L. baetica avoids interactions with ants, provokes strong aggression and, when found in ant nests, tends to occur at the periphery of the nest (Parmentier et al, 2022). (5) Unassociated: Allacrotelsa kraepelini and Ctenolepisma ciliatum normally do not live in ant nests, provoke a very strong aggression response, and therefore strictly avoid coming into contact with ants (Parmentier et al, 2022).…”

“…In contrast, another group of closely related Neoasterolepisma evolved specialized interactions with granivorous Messor ants. These myrmecophiles demonstrate the most advanced behavioural and chemical specializations within this genus and reside in the densest chambers of the nest (Parmentier et al, 2022).…”

“…The study of specialization in myrmecophiles primarily revolves around beetles (Parker, 2016;Valdivia et al, 2023;von Beeren et al, 2018), but a striking specialization continuum can also be found in silverfish, an early-branching group of wingless insects (Molero-Baltanás et al, 2017;Parmentier et al, 2022). One of the most remarkable groups is the radiated Neoasterolepisma genus (Zygentoma: Lepismatidae), exhibiting varying degrees of association with ants to obtain food.…”

“…Neoasterolepisma silverfish are particularly diverse in the Iberian peninsula (Molero-Baltanás et al, 2017). Obligate generalist Neoasterolepisma species such as N. curtiseta associate with multiple ant species and tend to forage at the periphery of ant colonies, hereby avoiding direct interactions with ant workers (Molero-Baltanás et al, 2017;Parmentier et al, 2022). In contrast, another group of closely related Neoasterolepisma evolved specialized interactions with granivorous Messor ants.…”