Chemical mimicry in an incipient leaf-cutting ant social parasite

Scientific Reports

In natural ecosystems, relationships between organisms are often characterised by high levels of complexity, where vulnerabilities in multi-trophic systems are difficult to identify, yet variation in specific community modules can be traceable. Within the complex community interactions, we can shed new light on dynamics by which co-evolutionary outcomes can inform science-led conservation. Here we assessed host-ant use in six populations of the butterfly Phengaris (=Maculinea) rebeli, an obligate social parasite of Myrmica ants and a model system in evolutionary and conservation ecology. Starting from the initial distribution of eggs, we estimated the survival of the parasite in the wild in nests of seven Myrmica ant species, and analysed the chemical cues evolved by the parasites to subvert its host defences. We found local variations in host specificity that are consistent with similarities found in the chemical profiles of hosts and parasites on different sites. At some sites, only one ant species is successfully exploited; at others, multiple-host populations are used. Understanding how stable or adaptable these associations are is essential knowledge when devising conservation measures to maintain keystone species of ant and locally adapted populations of Phengaris butterfly species, which are rare, threatened and a high priority for conservation worldwide. Although many generalist insect species can respond rapidly to environmental changes 1,2 , closely-coupled assemblages of interacting specialists are often more vulnerable, because survival may depend upon the maintenance of obligate co-adaptations or interactions within the community 3. An estimated ~100000 species of insect are myrmecophiles that interact with ants 4 ; most being facultative, often mutualistic, and displaying similar diffuse co-evolutionary patterns. About 10000 species are obligatory myrmecophiles, including many with antagonistic interactions in the form of social parasitism, where we expect to find tighter co-evolution between parasite and host, potentially in a geographical mosaic 5,6. The European Phengaris (=Maculinea) (P. arion, P. teleius, P. nausithous, P. alcon, P. rebeli-we considered the two latter taxa as separate following 7) are already the most studied ant-parasitic butterflies, and have become a model system in evolutionary and conservation ecology 8. P. rebeli adults, the focal species of this study, are on the wing from late June to mid-July and females oviposit on Gentiana cruciata. About four days after egg-laying, P. rebeli larvae hatch and feed for 10-14 days on their specific food plant. After the third moult, larvae leave the plant and drop to the ground where they are found by a Myrmica worker and carried into an ant nest 9. The adoption of caterpillars by ants is primarily mediated by chemical deception 6,10-13. As demonstrated for P. rebeli in SouthWestern Europe, pre-adoption caterpillars synthesise a simple mixture of surface hydrocarbons that weakly mimics those of Myrmica species in general, but has the closest match to the hydrocarbon signature of its host ant M. schencki 14. Yet the low level of chemical similarity, coupled with poor discrimination by foraging workers, means that P. rebeli pre-adoption caterpillars are retrieved into nests by workers of any foraging Myrmica species that happen to encounter them 10,11,14,15. Once inside ant colonies, the mimetic cocktail of hydrocarbons synthesised by caterpillars becomes more complex 11,15,16 , which, aided by acoustical mimicry 17-19 , not only enables the parasites to integrate closely with the societies of their primary ant host species but also identifies them as intruders to "non-host" species, where, in due course, either all or the large majority of individuals are killed or ejected by the more discriminatory nurse-workers 11,15,20,21 .

Animal Behaviour, 2015

Journal of Evolutionary Biology, 2005

Here we investigate the coevolutionary interactions between the slavemaking ant Protomognathus americanus and its Temnothorax hosts on a chemical level. We show that, although this social parasite is principally well-adapted to its hosts' cuticular hydrocarbon profile, there are pronounced differences in the fine-tuning of this adaptation. Between populations, chemical adaptation varies with host community composition, as the parasite faces a trade-off when confronted with more than one host species. In addition to adaptation of its own chemical signature, the slavemaker causes a reciprocal adjustment in its slaves' cuticular profile, the degree of which depends on the slave species. On the host side, successful parasite defence requires efficient enemy recognition, and in behavioural aggression trials, host colonies could indeed discriminate between invading slaves, which commonly accompany slavemakers on raids, and free-living conspecifics. Furthermore, hosts shifted their acceptance threshold over the seasons, presumably to reduce the costs of defence.

Evolutionary Ecology, 2010

Host-parasite coevolution shapes the structure of communities and simultaneously the traits of the interacting species. Social parasites developed sophisticated chemical integration strategies to circumvent host defences. Here, we show that the two Leptothorax host species of the obligate social parasite Harpagoxenus sublaevis exhibit extremely divergent chemical profiles, making it nearly impossible for this parasite to closely adapt to both hosts at once. Our cuticular hydrocarbon analyses demonstrate that H. sublaevis acquires some host chemicals passively, but additionally, actively biosyntheses some host hydrocarbons. The parasite adjusts thereby more closely to its smaller host, L. muscorum, because it actively produces two of its cuticular substances and also more easily acquires the short-chained hydrocarbons of this host. Community composition analyses indicate that the social parasite overexploits this chemical closer host species and, albeit costly for the parasite, frequently enslaves workers of the second host concurrently.

BMC Ecology, 2011

Background Social insects maintain the integrity of their societies by discriminating between colony members and foreigners through cuticular hydrocarbon (CHC) signatures. Nevertheless, parasites frequently get access to social resources, for example through mimicry of host CHCs among other mechanisms. The origin of mimetic compounds, however, remains unknown in the majority of studies (biosynthesis vs. acquisition). Additionally, direct evidence is scarce that chemical mimicry is indeed beneficial to the parasites (e.g., by improving social acceptance). Results In the present study we demonstrated that the kleptoparasitic silverfish Malayatelura ponerophila most likely acquires CHCs directly from its host ant Leptogenys distinguenda by evaluating the transfer of a stable-isotope label from the cuticle of workers to the silverfish. In a second experiment, we prevented CHC pilfering by separating silverfish from their host for six or nine days. Chemical host resemblance as well as ag...

American Naturalist, 2014

Social parasitism is defined by the exploitation of the social mechanisms of one society by another whole society. Here, we use quantitative ecological data and experiments to identify the components of a new form of social parasitism by the recently discovered “mirror turtle ant,” Cephalotes specularis. We show that C. specularis workers visually mimic and actively avoid contact with foragers of the hyperaggressive host ant Crematogaster ampla, allowing them to move freely in the extensive and otherwise defended foraging networks of host colonies. Workers from parasite colonies have immediate access to these networks by nesting exclusively within host territories, and 89% of all potential host territories were parasitized. Inside the network, parasite workers eavesdrop on the host’s trail pheromones to locate and exploit food resources that are defended by the host to the exclusion of all other ants. Experiments demonstrated the unprecedented capacity of the parasite for superior foraging performance on its host’s pheromone trails than on trails of its own. Considered together, the apparent Batesian-Wallacian mimicry, pheromone-based interceptive eavesdropping, kleptoparasitism, and xenobiotic nesting ecology displayed by C. specularis within the territory and foraging network of a host ant represents a novel adaptive syndrome for social exploitation.

Proceedings of the Royal Society B: Biological Sciences, 2007

Social parasites are involved in a coevolutionary arms race, which drives increasing specialization resulting in a very narrow host range. The Formicoxenus ants are a small group of social parasites with a xenobiotic lifestyle. Formicoxenus quebecensis and Formicoxenus provancheri are highly specialized ants using chemical mimicry to blend into their respective Myrmica ant host colonies. However, Formicoxenus nitidulus is unique in being able to survive in over 11 different ant host species. We observed that when live or dead F. nitidulus adults are seized by their host they are immediately dropped undamaged, despite possessing a cuticular hydrocarbon profile that differs markedly from its host. Hexane extracts of the F. nitidulus cuticle made previously acceptable prey items unattractive to their Formica host, indicating a chemical deterrent effect. This is the first time that a social parasite has been shown to exploit the generalized deterrence strategy to avoid host aggression over long periods of time. This supports the idea that coevolved and generalist diseases or parasites require fundamentally different defence mechanisms. We suggest that F. nitidulus uses its cuticular chemistry, possible alkadienes, as a novel deterrent mechanism to allow it to switch hosts easily and so become a widespread and abundant social parasite.

Journal of Insect Physiology, 2015

Communication in ants is based to a great extent on chemical compounds. Recognition of intruders is primarily based on cuticular hydrocarbon (CHC) profile matching but is prone to being cheated. Eucharitid wasps are specific parasitoids of the brood of ants; the immature stages are either well integrated within the colony or are protected within the host cocoons, whereas adult wasps at emergence must leave their host nest to reproduce and need to circumvent the ant recognition system to escape unscathed. The behavioral interactions between eucharitid wasps and workers of their host, the Neotropical ant Ectatomma tuberculatum, are characterized. In experimental bioassays, newly emerged parasitoids were not violently aggressed. They remained still and were grabbed by ants upon contact and transported outside the nest; host workers were even observed struggling to reject them. Parasitoids were removed from the nest within five minutes, and most were unharmed, although two wasps (out of 30) were killed during the interaction with the ants. We analyzed the CHCs of the ant and its two parasitoids, Dilocantha lachaudii and Isomerala coronata, and found that although wasps shared all of their compounds with the ants, each wasp species had typical blends and hydrocarbon abundance was also species specific. Furthermore, the wasps had relatively few CHCs compared to E. tuberculatum (22-44% of the host components), and these were present in low amounts. Wasps, only partially mimicking the host CHC profile, were immediately recognized as alien and actively removed from the nest by the ants. Hexane-washed wasps were also transported to the refuse piles, but only after being thoroughly inspected and after most of the workers had initially ignored them. Being recognized as intruder may be to the parasitoids' advantage, allowing them to quickly leave the natal nest, and therefore enhancing the fitness of these very short lived parasitoids. We suggest that eucharitids take advantage of the hygienic behavior of ants to quickly escape from their host nests.

Proceedings of the Royal Society of London. Series B: Biological Sciences, 1999

Although it has always been assumed that chemical mimicry and camou£age play a major role in the penetration of ant societies by social parasites, this paper provides the ¢rst direct evidence for such a mechanism between the larvae of the parasitic butter£y Maculinea rebeli and its ant host Myrmica schencki. In the wild, freshly moulted fourth-instar caterpillars, which have no previous contact with ants, appear to be recognized as ant larvae by foraging Myrmica workers, which return them to their nest brood chambers. Three hypotheses concerning the mechanism controlling this behaviour were tested: (i) the caterpillars produce surface chemicals that allow them to be treated as ant larvae; (ii) mimetic compounds would include hydrocarbons similar to those employed by Myrmica to recognize conspeci¢cs and brood; and (iii) the caterpillars' secretions would more closely mimic the pro¢le of their main host in the wild, M. schencki, than that of other species of Myrmica. Results of behavioural bioassays and chemical analyses con¢rmed all three hypotheses, and explained the high degree of host speci¢city found in this type of highly specialized myrmecophile. Furthermore, although caterpillars biosynthesized many of the recognition pheromones of their host species (chemical mimicry), they later acquired additional hydrocarbons within the ant nest (chemical camou£age), making them near-perfect mimics of their individual host colony's odour.

Revista Brasileira de Entomologia, 2017

Social animals are faced with an intriguing dilemma. On the one hand, interactions between individuals are essential to exchange information and to promote cohesion, while on the other hand such interactions carry with them the risk of catching and transmitting parasites. This trade-off is particularly significant for social insects because low within-colony genetic diversity makes their colonies potentially vulnerable to parasites while frequent interactions are essential to the development of the colonial odor profile necessary for nestmate recognition. Here we investigate whether social interactions between young and old leaf-cutting ant workers show evidence of this trade-off. We find that old workers engage in more selfgrooming and mandibular scraping than young workers, both in keeping with old workers having been more exposed to parasites. In contrast, we find that young workers engaged in more allogrooming than old workers, which seems likely to have a different motivation possibly the transfer of recognition cues. Furthermore, young workers tended to engage in allogrooming with other young workers, although it was the old workers that were most active and with whom allogrooming would seem likely to optimize information or chemicals transfer. This suggests that young workers may be attempting to minimize the risk of parasite transmission during their social interactions. Although limited to behavioral data, these results hint that ant workers may be sensitive to the trade-off between the transmission of recognition cues and disease, and adjust their social interactions accordingly.