Ants dominate terrestrial ecosystems through living in complex societies whose organization is maintained via sophisticated communication systems. The role of acoustics in information exchange may be underestimated. We show that Myrmica schencki queens generate distinctive sounds that elicit increased benevolent responses from workers, reinforcing their supreme social status. Although fiercely defended by workers, ant societies are infiltrated by specialist insects that exploit their resources. Sounds produced by pupae and larvae of the parasitic butterfly Maculinea rebeli mimic those of queen ants more closely than those of workers, enabling them to achieve high status within ant societies. We conclude that acoustical mimicry provides another route for infiltration for ∼10,000 species of social parasites that cheat ant societies.

SUMMARY: Rapid, effective communication between colony members is a key attribute that enables ants to live in dominant, fiercely protected societies. Their signals, however, may be mimicked by other insects that coexist as commensals with ants or interact with them as mutualists or social parasites. We consider the role of acoustics in ant communication and its exploitation by social parasites. Social parasitism has been studied mainly in the butterfly genus Maculinea, the final instar larvae of which are host-specific parasites of Myrmica ants, preying either on ant grubs (predatory Maculinea) or being fed by trophallaxis (cuckoo Maculinea). We found similar significant differences between the stridulations of model queen and worker ant castes in both Myrmica sabuleti and Myrmica scabrinodis to that previously reported for Myrmica schencki. However, the sounds made by queens of all three Myrmica species were indistinguishable, and among workers, stridulations did not differ significantly in two of three species-pairs tested. Sounds recorded from the predatory caterpillars and pupae of Maculinea arion had similar or closer patterns to the acoustics of their host Myrmica sabuleti than those previously reported for the cuckoo Maculinea rebeli and its host Myrmica schencki, even though Maculinea rebeli caterpillars live more intimately with their host. We conclude that chemical mimicry enables Maculinea larvae to be accepted as colony members by worker ants, but that caterpillars and pupae of both predatory and cuckoo butterflies employ acoustical mimicry of queen ant calls to elevate their status towards the highest attainable position within their host's social hierarchy.

About 10,000 arthropods live as ants' social parasites and have evolved a number of mechanisms allowing them to penetrate and survive inside the ant nests. Many of them can intercept and manipulate their host communication systems. This is particularly important for butterflies of the genus Maculinea, which spend the majority of their lifecycle inside Myrmica ant nests. Once in the colony, caterpillars of Maculinea “predatory species” directly feed on the ant larvae, while those of “cuckoo species” are fed primarily by attendance workers, by trophallaxis. It has been shown that Maculinea cuckoo larvae are able to reach a higher social status within the colony's hierarchy by mimicking the acoustic signals of their host queen ants. In this research we tested if, when and how myrmecophilous butterflies may change sound emissions depending on their integration level and on stages of their life cycle. We studied how a Maculinea predatory species (M. teleius) can acoustically interact with their host ants and highlighted differences with respect to a cuckoo species (M. alcon). We recorded sounds emitted by Maculinea larvae as well as by their Myrmica hosts, and performed playback experiments to assess the parasites' capacity to interfere with the host acoustic communication system. We found that, although varying between and within butterfly species, the larval acoustic emissions are more similar to queens' than to workers' stridulations. Nevertheless playback experiments showed that ant workers responded most strongly to the sounds emitted by the integrated (i.e. post-adoption) larvae of the cuckoo species, as well as by those of predatory species recorded before any contact with the host ants (i.e. in pre-adoption), thereby revealing the role of acoustic signals both in parasite integration and in adoption rituals. We discuss our findings in the broader context of parasite adaptations, comparing effects of acoustical and chemical mimicry.

There is increasing evidence that most parapatric cryptic/sister taxa are reproductively compatible across their areas of contact. Consequently, the biological species concept, which assumes absence of interbreeding, is becoming a not so effective criterion in evolutionary ecology. Nevertheless, the few parapatric sister taxa showing complete reproductive barriers represent interesting models to study speciation processes and the evolution of reproductive isolation. In this study, we examined contact populations in northwestern Italy of two butterfly species, Zerynthia polyxena and Z. cassandra , characterized by different genitalic morphotypes. We studied levels of divergence among 21 populations distributed from Sicily to France using three genetic markers (the mitochondrial COI and ND1 genes and the nuclear wingless gene) and genitalic geometric morphometrics. Moreover, we performed species distribution modelling to estimate different climatic requirements of Z. polyxena and Z. cassandra . We projected climatic data into glacial maximum scenarios in order to verify if and to which extent glacial cycles could have contributed to speciation processes. Genetic and morphometric analyses identified two main groups. All specimens showed a concordant pattern of diversification, including those individuals sampled in the contact area. Haplotype distribution and climatic models showed that during glacial maxima both species experienced a strong range contraction and presumably remained separated into different microrefugia in southern France, in the Italian Peninsula and on the islands of Elba and Sicily. Long term separation was probably favoured by reduced dispersal ability and high phylopatry, while genitalic diversification probably favoured interbreeding avoidance. Conversely, the aposematic wing pattern remained almost identical. We compared our results with those obtained in other species and concluded that Z. polyxena and Z. cassandra represent a valuable model in the study of speciation.