Francesca Barbero

Queen ants make distinctive sounds that are mimicked by a butterfly social parasite.

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.

Relative importance of density-dependent regulation and environmental stochasticity for butterfly population dynamics

The relative contribution of density-dependent regulation and environmental stochasticity to the temporal dynamics of animal populations is one of the central issues of ecology. In insects, the primary role of the latter factor, typically represented by weather patterns, is widely accepted. We have evaluated the impact of density dependence as well as density-independent factors, including weather and mowing regime, on annual fluctuations of butterfly populations. As model species, we used Maculinea alcon and M. teleius living in sympatry and, consequently, we also analysed the effect of their potential competition. Density dependence alone explained 62 and 42% of the variation in the year-to-year trends of M. alcon and M. teleius, respectively. The cumulative Akaike weight of models with density dependence, which can be interpreted as the probability that this factor should be contained in the most appropriate population dynamics model, exceeded 0.97 for both species. In contrast, the impacts of inter-specific competition, mowing regime and weather were much weaker, with their cumulative weights being in the range of 0.08–0.21; in addition, each of these factors explained only 2–5% of additional variation in Maculinea population trends. Our results provide strong evidence for density-dependent regulation in Maculinea, while the influence of environmental stochasticity is rather minor. In the light of several recent studies on other butterflies that detected significant density-dependent effects, it would appear that density-dependent regulation may be more widespread in this group than previously thought, while the role of environmental stochasticity has probably been overestimated. We suggest that this misconception is the result of deficiencies in the design of most butterfly population studies in the past, including (1) a strong focus on adults and a neglect of the larval stage in which density-dependent effects are most likely to occur; (2) an almost exclusive reliance on transect count results that may confound the impact of environmental stochasticity on butterfly numbers with its impact on adult longevity.

Acoustical mimicry in a predatory social parasite of ants.

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 hosts social hierarchy.

Myrmica ants host highly diverse parasitic communities: from social parasites to microbes

Myrmica ants have been model species for studies in a variety of disciplines, including insect physiology, chemical communication, ant social dynamics, ant population, community ecology, and ant interactions with other organisms. Species belonging to the genus Myrmica can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and systematics have been thoroughly studied. These ants serve as hosts to highly diverse parasitic organisms from socially parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in colony fitness. A comprehensive review of the parasitic organisms supported by Myrmica and the effects of these organisms on individuals and on whole ant colonies has not yet been compiled. Here, we provide a review of the interactions of these organisms with Myrmica ants by discussing host and parasite functional, behavioral or physiological adaptations. In addition, for all “symbiont groups” of Myrmica ants described in this paper, we examine the present limitations of the knowledge at present of their impact on individuals and host colony fitness. In conclusion, we argue that Myrmica ants serve as remarkable resource for the evolution of a wide variety of associated organisms.

Selection on dispersal in isolated butterfly metapopulations

In most metapopulation models dispersal is assumed to be a fixed species-specific trait, but in reality dispersal abilities are highly sensitive to various selective pressures. Strict isolation of a metapopulation, which precludes any influx of immigrants (and their genes) from outside and makes it impossible for emigrants to reach other localities with suitable habitat, thus reducing fitness benefits of long-distance dispersal to zero, may be expected to impose strong selection against dispersal. We tested the above prediction by comparing dispersal parameters derived with the Virtual Migration model for isolated and non-isolated metapopulations of two species of large blue Maculinea (= Phengaris) butterflies, surveyed with intensive mark-recapture. Mortality during dispersal was found to be twice (in M. teleius) to five times higher (in M. arion) in isolated metapopulations. Isolation also resulted in significantly reduced dispersal distances in isolated metapopulations, with the effect being particularly strong in M. arion females. Apart from its evolutionary and ecological consequences, dispersal depression in isolated butterfly metapopulations implied by our results has serious conservation implications. It provides a clear argument against using parameter values obtained in a different environmental setting in modelling applications, e.g., Population Viability Analyses or environmental impact assessment. Furthermore, it underlines the importance of establishing well-connected networks of suitable habitats prior to species release in areas where reintroductions are planned.

The “Evolutionarily Significant Unit” concept and its applicability in biological conservation

Abstract Although most conservationists claim to protect “species”, the conservation unit actually and practically managed is the individual population. As resources are not unlimited, we need to focus on a restricted number of populations. But how can we select them? The Evolutionarily Significant Unit (ESU), first conceptualised by Ryder in 1986, may offer some answer. Several definitions have been proposed for the ESU, but all make reference to units “whose divergence can be measured or evaluated by putting differential emphasis on the role of evolutionary forces at varied temporal scales”. Thus, an ESU might be fully identical with a “species”, or a “species” could be composed of multiple ESUs. On the other hand, an ESU might comprise single/multiple populations exchanging a degree of gene flow, such as meta-populations. In an attempt to show strengths and weaknesses of ESU concepts, we present here, among several others, some case studies on the myrmecophilous butterflies of the genus Maculinea. In particular, we analyse the apparently everlasting debate about Maculinea alcon and M. rebeli, whose separation into separate species has been accepted by many authors, on mainly ecological criteria, but has not been fully supported by molecular analyses. We also discuss how the tight association with host ants may have driven selection for increasingly more strictly adapted Maculinea populations, arguably deserving specific taxonomic identity. Finally we discuss how current DNA analyses may fail to detect critical information on differences between taxa recently originated by the action of separate adaptive processes, which non-molecular studies can sometimes reveal. We conclude by discussing some current and often conflicting taxonomic trends, in their relationships with conservation policies.

Corruption of ant acoustical signals by mimetic social parasites: Maculinea butterflies achieve elevated status in host societies by mimicking the acoustics of queen ants

Recent recordings of the stridulations of Myrmica ants revealed that their queens made distinctive sounds from their workers, although the acoustics of queens and workers, respectively, were the same in different species of Myrmica. Queen recordings induced enhanced protective behavior when played to workers in the one species tested. Larvae and pupae of the butterfly genus Maculinea inhabit Myrmica colonies as social parasites, and both stages generate sounds that mimic those of a Myrmica queen, inducing similar superior treatments from workers as their model. We discuss how initial penetration and acceptance as a colony member is achieved by Maculinea through mimicking the species-specific semio-chemicals of their hosts, and how acoustical mimicry is then employed to elevate the parasite’s membership of that society towards the highest attainable level in their host’s hierarchy. We postulate that, if acoustics is as well developed a means of communication in certain ants as these studies suggest, then others among an estimated 10,000 species of ant social parasite may supplement their well-known use of chemical and tactile mimicry to trick host ants with mimicry of host acoustical systems.

Plant defences against ants provide a pathway to social parasitism in butterflies

Understanding the chemical cues and gene expressions that mediate herbivore–host-plant and parasite–host interactions can elucidate the ecological costs and benefits accruing to different partners in tight-knit community modules, and may reveal unexpected complexities. We investigated the exploitation of sequential hosts by the phytophagous–predaceous butterfly Maculinea arion, whose larvae initially feed on Origanum vulgare flowerheads before switching to parasitize Myrmica ant colonies for their main period of growth. Gravid female butterflies were attracted to Origanum plants that emitted high levels of the monoterpenoid volatile carvacrol, a condition that occurred when ants disturbed their roots: we also found that Origanum expressed four genes involved in monoterpene formation when ants were present, accompanied by a significant induction of jasmonates. When exposed to carvacrol, Myrmica workers upregulated five genes whose products bind and detoxify this biocide, and their colonies were more tolerant of it than other common ant genera, consistent with an observed ability to occupy the competitor-free spaces surrounding Origanum. A cost is potential colony destruction by Ma. arion, which in turn may benefit infested Origanum plants by relieving their roots of further damage. Our results suggest a new pathway, whereby social parasites can detect successive resources by employing plant volatiles to simultaneously select their initial plant food and a suitable sequential host.

Contrasting genetic structure of rear edge and continuous range populations of a parasitic butterfly infected by Wolbachia

BackgroundClimatic oscillations are among the long-term factors shaping the molecular features of animals and plants and it is generally supposed that the rear edges (i.e., the low-latitude limits of distribution of any given specialised species) situated closer to glacial refugia are vital long-term stores of genetic diversity. In the present study, we compared the genetic structure of several populations of an endangered and obligate myrmecophilous butterfly (Maculinea arion) from two distinct and geographically distant parts of its European distribution (i.e., Italy and Poland), which fully represent the ecological and morphological variation occurring across the continent.ResultsWe sequenced the COI mitochondrial DNA gene (the ‘barcoding gene’) and the EF-1α nuclear gene and found substantial genetic differentiation among M. arion Italian populations in both markers. Eleven mtDNA haplotypes were present in Italy. In contrast, almost no mtDNA polymorphisms was found in the Polish M. arion populations, where genetic differentiation at the nuclear gene was low to moderate. Interestingly, the within-population diversity levels in the EF-1α gene observed in Italy and in Poland were comparable. The genetic data did not support any subspecies divisions or any ecological specialisations. All of the populations studied were infected with a single strain of Wolbachia and our screening suggested 100% prevalence of the bacterium.ConclusionsDifferences in the genetic structure of M. arion observed in Italy and in Poland may be explained by the rear edge theory. Although we were not able to pinpoint any specific evolutionarily significant units, we suggest that the Italian peninsula should be considered as a region of special conservation concern and one that is important for maintaining the genetic diversity of M. arion in Europe. The observed pattern of mtDNA differentiation among the populations could not be explained by an endosymbiotic infection.

Butterflies that trick ants with sound

Larvae of parasitic Maculinea butterflies use acoustic mimicry to induce host ants to adopt and care for them.