Obligate Social Parasite Research Articles

Mitochondrial phylogenomics of bumblebees, Bombus (Hymenoptera: Apidae): a tale of structural variation, shifts in selection constraints, and tree discordance

Abstract The mitochondrial DNA (mtDNA) of bumblebees (Bombus) has been widely used for phylogenetic studies, but its evolution is still underexplored. Here we report a comprehensive analysis of 60 bumblebee mitogenomes, including 40 newly assembled ones, to investigate bumblebee mtDNA structure, composition, and informativeness under a phylogenetic framework. Our mtDNA dataset supports the monophyly of Bombus and its subgenera, although we found a high degree of tree discordance in deeper nodes when using different inference methods or matrix composition. Concerning mitogenome structure, our results show that tRNA genes were often rearranged, with unique rearrangements indicating shared ancestry across bumblebee subgenera, illustrating their potential for subgeneric classification. Our results also challenge the notion that faster evolving mtDNA exhibits higher gene rearrangement rates. Finally, we explicitly assessed shifts in selection constraints of mtDNA genes in obligate social parasites of subgenus Psithyrus and found that their mtDNA evolved under relaxed selective constraints. Our findings show the utility of mtDNA in providing insights into bumblebee phylogenetics, evolution, and genome trait diversification. We also highlight the potential for comparative mitogenomics to uncover previously unknown aspects of bumblebee evolution, offering exciting opportunities for future research in this field.

Brain and antennal transcriptomes of host ants reveal potential links between behaviour and the functioning of socially parasitic colonies.

Insect social parasites are characterized by exploiting the hosts' social behaviour. Why exactly hosts direct their caring behaviour towards these parasites and their offspring remains largely unstudied. One hypothesis is that hosts do not perceive their social environment as altered and accept the parasitic colony as their own. We used the ant Leptothorax acervorum, host of the dulotic, obligate social parasite Harpagoxenus sublaevis, to shed light on molecular mechanisms underlying behavioural exploitation by contrasting tissue-specific transcriptomes in young host workers. Host pupae were experimentally (re-)introduced into fragments of their original, another conspecific, heterospecific or parasitic colony. Brain and antennal mRNA was extracted and sequenced from adult ants after they had lived in the experimental colony for at least 50 days after eclosion. The resulting transcriptomes of L. acervorum revealed that ants were indeed affected by their social environment. Host brain transcriptomes were altered by the presence of social parasites, suggesting that the parasitic environment influences brain activity, which may be linked to behavioural changes. Transcriptional activity in the antennae changed most with the presence of unrelated individuals, regardless of whether they were conspecifics or parasites. This suggests early priming of odour perception, which was further supported by sensory perception of odour as an enriched function of differentially expressed genes. Furthermore, gene expression in the antennae, but not in the brain corresponded to ant worker behaviour before sampling. Our study demonstrated that the exploitation of social behaviours by brood parasites correlates with transcriptomic alterations in the central and peripheral nervous systems.

A new host for a new Rossomyrmex minuchae population

Social parasites usually rely on chemical cues (cuticular hydrocarbons) to successfully invade and coexist with their hosts. Most ants that are obligate social parasites (slave-makers) can parasitize several related host species with different levels of chemical similarity although there are few exceptions where there is only a single host species. An example of the latter is Rossomyrmex minuchae, which was known to be only associated with Proformica longiseta. However, a recent discovery of a new R. minuchae population revealed that it can parasitize P. nasuta, a species with a separate distribution to P. longiseta. Chemical analyses of cuticular hydrocarbons show local adaptation of the parasite to its host in this new population, being more similar to P. nasuta than to other R. minuchae populations. In addition, genetic analyses evidence differences from the other known populations, from which it split 1.21 Mya during glacial and interglacial periods of the Pleistocene and remained separated to the present day. This historical genetic isolation and the chemical differences found between parasite populations may evidence a speciation process and support the local host–parasite coevolution.

Does effective population size affect rates of molecular evolution: Mitochondrial data for host/parasite species pairs in bees suggests not.

Adaptive evolutionary theory argues that organisms with larger effective population size (N e) should have higher rates of adaptive evolution and therefore greater capacity to win evolutionary arm races. However, in some certain cases, species with much smaller N e may be able to survive besides their opponents for an extensive evolutionary time. Neutral theory predicts that accelerated rates of molecular evolution in organisms with exceedingly small N e are due to the effects of genetic drift and fixation of slightly deleterious mutations. We test this prediction in two obligate social parasite species and their respective host species from the bee tribe Allodapini. The parasites (genus Inquilina) have been locked into tight coevolutionary arm races with their exclusive hosts (genus Exoneura) for ~15 million years, even though Inquilina exhibit N e that are an order of magnitude smaller than their host. In this study, we compared rates of molecular evolution between host and parasite using nonsynonymous to synonymous substitution rate ratios (dN/dS) of eleven mitochondrial protein‐coding genes sequenced from transcriptomes. Tests of selection on mitochondrial genes indicated no significant differences between host and parasite dN/dS, with evidence for purifying selection acting on all mitochondrial genes of host and parasite species. Several potential factors which could weaken the inverse relationship between N e and rate of molecular evolution are discussed.

Differential investment in visual and olfactory brain regions is linked to the sensory needs of a wasp social parasite and its host.

Obligate insect social parasites evolve traits to effectively locate and then exploit their hosts, whereas hosts have complex social behavioral repertoires, which include sensory recognition to reject potential conspecific intruders and heterospecific parasites. While social parasites and host behaviors have been studied extensively, less is known about how their sensory systems function to meet their specific selective pressures. Here, we compare investment in visual and olfactory brain regions in the paper wasp Polistes dominula, and its obligate social parasite P. sulcifer, to explore the links among sensory systems,brain and behavior. Our results show significant relative volumetric differences between these two closely related species, consistent with their very different life histories. Social parasites show proportionally larger optic lobes and central complex to likely navigate long-distance migrations and unfamiliar landscapes to locate the specific species of hosts they usurp. Contrastingly, hosts have larger antennal lobes and calyces of the mushroom bodies compared with social parasites, as predicted by their sensory means to maintain social cohesion via olfactory signals, allocate colony tasks, forage, and recognize conspecific and heterospecific intruders. Our work suggests how this tradeoff between visual and olfactory brain regions may facilitate different sensory adaptations needed to perform social and foraging tasks by the host, including recognition of parasites, or to fly long distances and successful host localizing by the social parasite.

Relaxed selection underlies genome erosion in socially parasitic ant species

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches.

Range expansion in an introduced social parasite-host species pair

Dispersal in social parasites is constrained by the presence of suitable host populations, limiting opportunities for rapid range expansion. For this reason, although hundreds of ant species have expanded their ranges through human transport, few obligate social parasites have done so. We test the hypothesis that social parasites expand their ranges more slowly than their hosts by examining the spread of an introduced social parasite-host species pair in North America—the workerless ant Tetramorium atratulum and the pavement ant T. immigrans. In doing so we report a new range extension of T. atratulum in the interior US. Consistent with host limitation on dispersal, we found a time lag ranging from several years to over a century between the arrivals of the host and parasite to a new region. The estimated maximum rate of range expansion in the parasite was only a third as fast as that of the host. We suggest that relative to free-living social insects, social parasites may be less able to rapidly shift their ranges in response to changes in habitat or climate.

Host specificity pattern and chemical deception in a social parasite of ants

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.

Appeasing their hosts: a novel strategy for parasite brood

Brood and social parasites exploit the parental care of their host and often integrate into host colonies using different strategies at different moments during their life cycle. In social wasps, the obligate social parasite Polistes atrimandibularis, using chemical mimicry and chemical insignificance, avoids detection by its host, Polistes biglumis, which has an efficient nestmate recognition system. Enslaved host foundresses accept and care for parasite brood as if it were their own. This observation raises the following question: how exactly do parasite brood escape detection and increase host acceptance? Here, we compared the cuticular chemical signatures of parasite brood and host brood. Their signatures differed in composition: parasite larvae and pupae had particularly high levels of alkenes (notably 9-nonacosene), which were absent in host larvae and pupae. Given this result, we tested the effect of 9-nonacosene on host foundresses, and documented that they reduced their aggression. Our findings address a novel integration strategy for social parasite brood as they suggest that the hydrocarbon serves as an appeasement substance and promotes host tolerance of parasite larvae and pupae, which are chemically disparate from host larvae and pupae.

Genetic and chemical divergence among host races of a socially parasitic ant.

Host–parasite associations facilitate the action of reciprocal selection and can drive rapid evolutionary change. When multiple host species are available to a single parasite, parallel specialization on different hosts may promote the action of diversifying natural selection and divergence via host race formation. Here, we examine a population of the kidnapper ant (Polyergus mexicanus) that is an obligate social parasite of three sympatric ant species: Formica accreta, F. argentea, and F. subaenescens (formerly F. fusca). Behavioral and ecological observations of P. mexicanus have shown that individual colonies parasitize only one species of host and that new Polyergus queens maintain host fidelity when establishing new colonies. To successfully adapt to a particular host, Polyergus ants may mimic or camouflage themselves with the species‐specific chemical cues (cuticular hydrocarbons) that their hosts use to ascertain colony membership. To investigate the extent of host specialization, we collected both genetic and chemical data from P. mexicanus that parasitize each of the three different Formica species in sympatry. We show that host‐associated genetic structure exists for both maternally inherited mitochondrial DNA data and biparentally inherited microsatellite markers. We also show that P. mexicanus can be distinguished by chemical profile according to host due to partial matching with their host. Our results support the hypothesis that host race formation is occurring among lineages of P. mexicanus that use different Formica hosts. Thus, this system may represent a promising model for illuminating the early steps of divergence, accumulation of reproductive isolation, and speciation.

Sex Ratios in a Socially Parasitic Bee and Implications for Host-Parasite Interactions

Obligate social parasites of Hymenoptera, known as inquilines, have received enormous attention due to the elaborate adaptations they exhibit for exploiting their hosts, and because they have frequently been used to infer sympatric speciation. Their population biology can be difficult to infer as they are both rare and difficult to extract from host nests. Sex allocation has been studied for very few inquilines of social Hymenoptera. Here we report sex ratio patterns in the allodapine bee Inquilina schwarzi, which is an obligate social parasite of another allodapine, Exoneura robusta. We show that the sex ratio of this inquiline varies with its brood number, it is female-biased in the smallest broods, but becomes more even in larger broods, where the population-wide sex ratio is close to parity. We argue that this pattern of bias is consistent with local resource competition, where inquiline females compete to inherit their natal colony. We also argue that extremely female-biased sex ratios of the host species, combined with overall sex ratio parity in the parasite, may help ameliorate disparity in effective population sizes between these two species which are locked in an evolutionary arms race.

A scent shield to survive: identification of the repellent compounds secreted by the male offspring of the cuckoo bumblebee Bombus vestalis

AbstractIn social insects, the high cost of parental investment has promoted the evolution of traits that reduce or avoid care for unrelated offspring. They have evolved a sophisticated recognition system which enables them to reject foreign individuals, and therefore prevent their nest's exploitation by parasites and predators. Nonetheless, many social parasites are able to overcome social insect recognition and parasitize their parental care behaviour by laying their eggs in host nests. Although several studies have already been conducted on the strategies used by social parasites to successfully invade host nests, the strategy used by its offspring to evade host rejection is still poorly understood. In bumblebees, previous investigations indicated that male offspring of Bombus vestalis (Geoffroy) (Hymeno‐ptera: Apidae), the specific obligate social parasite of Bombus terrestris (L.), may use allomones to evade host worker attacks. Following these studies, we performed electrophysiological studies and behavioural experiments to identify the potential repellents. Six compounds elicited electroantennographic responses in host worker antennae. The corresponding mixture of synthetic volatiles as well as pure tetradecyl acetate, and to a lesser extent pure (Z)‐11‐hexadecenyl acetate, showed a repellent effect on starved host workers in a feeding bioassay. We hypothesize that tetradecyl acetate has a key function in the repellent effect of the secretions of B. vestalis male offspring towards B. terrestris host workers.

Phylogenetic tests reject Emery's rule in the evolution of social parasitism in yellowjackets and hornets (Hymenoptera: Vespidae, Vespinae).

Social parasites exploit the brood-care behaviour and social structure of one or more host species. Within the social Hymenoptera there are different types of social parasitism. In its extreme form, species of obligate social parasites, or inquilines, do not have the worker caste and depend entirely on the workers of a host species to raise their reproductive offspring. The strict form of Emery's rule states that social parasites share immediate common ancestry with their hosts. Moreover, this rule has been linked with a sympatric origin of inquilines from their hosts. Here, we conduct phylogenetic analyses of yellowjackets and hornets based on 12 gene fragments and evaluate competing evolutionary scenarios to test Emery's rule. We find that inquilines, as well as facultative social parasites, are not the closest relatives of their hosts. Therefore, Emery's rule in its strict sense is rejected, suggesting that social parasites have not evolved sympatrically from their hosts in yellowjackets and hornets. However, the relaxed version of the rule is supported, as inquilines and their hosts belong to the same Dolichovespula clade. Furthermore, inquilinism has evolved only once in Dolichovespula.

Acromyrmex charruanus: a new inquiline social parasite species of leaf-cutting ants

Social parasites exploit the colony resources of social species to secure their own survival and reproduction. Social parasites are frequently studied as models for conflict and cooperation as well as for speciation. The eusocial Hymenoptera harbor a diverse array of socially parasitic species with idiosyncratic life history strategies, but it is probably in the ants where social parasites are most speciose and have evolved the highest degrees of morphological and behavioral specialization. In the fungus-growing ants, a total of five obligate social parasites are known: four species are parasites of leaf-cutting ants and one species parasitizes a primitive fungus-growing ant species in the genus Mycocepurus. Here we describe a new species of socially parasitic leaf-cutting ant, Acromyrmex charruanus sp. nov., from Uruguay, and we report initial observations on the parasite’s life history as well as on the morphological and behavioral adaptations related to the inquiline syndrome. Our observations suggest that Acromyrmex charruanus is an obligate inquiline social parasite of the thatch-mound-building, leaf-cutting ant Acromyrmex heyeri. Acromyrmex charruanus appears to be tolerant of the host, producing sexual offspring in the presence of the A. heyeri host queen. Queens of A. charruanus appear to reproduce semelparously and sexual offspring are produced during the austral fall (February), which differs significantly from the mating biology of the host species, which reproduces during the southern-hemisphere spring (October–December). We suggest that the diametrically opposed mating seasons of parasite and host might be adaptive, allowing the parasite to avoid competition for resources with the host sexual brood. The morphological and behavioral adaptations of A. charruanus accord with characters observed to arise early during the evolution of other ant inquiline parasite species, and so far we have no evidence for the existence of a worker caste in A. charruanus. Further field studies and behavioral experiments need to confirm our first observations and explore A. charruanus’s behavioral ecology, evolution, and life history in more detail.

Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra.

Pairs of obligate social parasites and their hosts, where some of the parasites have recently diverged from their host through intraspecific social parasitism, provide intriguing systems for studying the modes and processes of speciation. Such speciation, probably in sympatry, has also been propounded in the ant Myrmica rubra and its intraspecific social parasite. In this species, parasitism is associated with queen size dimorphism, and the small microgyne has become a social parasite of the large macrogyne. Here, we investigated the genetic divergence of the host and the parasite queen morphs in 11 localities in southern Finland, using nuclear and mitochondrial markers of queens and workers. We formulated and tested four speciation-related hypotheses that differed in the degree of genetic divergence between the morphs. The queen morphs were genetically distinct from each other with little hybridization. In the nuclear data, when localities were nested within queen morphs in the hierarchical amova, 39% of the genetic variation was explained by the queen morph (standardized F'CT = 0.63, uncorrected FCT = 0.39), whereas 18% was explained by the locality (F'SC = 0.39, FSC = 0.29). This result corroborated the hypothesis of advanced sympatric speciation. In contrast, the mitochondrial DNA could not settle between the hierarchical levels of locality and queen morph, thus substantiating equally the hypotheses of incipient and advanced sympatric speciation. Together, our results support the view that the microgynous parasite has genetically diverged from its macrogynous host to the level of a nascent species.

Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

Brain investment is evolutionarily constrained by high costs of neural tissue. Several ecological factors favour the evolution of increased brain investment; we predict reduced brain region investment will accompany the evolution of organismal or social parasitism when parasites rely on host behaviour and cognition to solve ecological problems. To test this idea we investigated whether brain region investments differed between obligate slave-making Polyergus mexicanus ant workers and their Formica fusca slave workers. Polyergus workers perform little labour for their colonies; enslaved workers of Formica host species forage, excavate nests and tend the brood. We focused on the calyces of the mushroom bodies, central processing brain regions that are larger in social insect workers that perform complex tasks. As predicted we found lower relative investment in mushroom body calyx in P. mexicanus workers than in F. fusca workers; by contrast, enslaved and free F. fusca workers did not differ in mushroom body calyx volume. We then tested whether slave-makers and hosts differed in brain investment among sensory modalities. Polyergus slave-makers employ several unique classes of pheromones during raids, and eye size relative to head size was smaller in P. mexicanus workers than in F. fusca workers. The size of antennal brain tissues relative to visual tissues was greater in Polyergus, both in the peripheral sensory lobes and in the mushroom body calyx, suggesting greater relative investment in antennal processing by slave-makers. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 415–422.

Cuckoo wasps manipulate foraging and resting activities in their hosts

Parasite-induced alterations in host behaviour have been reported in a large number of taxa. However, some parasites are better than others to exploit the resources offered by their hosts. To date, our understanding of the extent to which some obligate parasites exploit social insect colonies is still limited. In this study, we examined parasite-mediated behavioural alterations of Polistes biglumis wasps parasitized by the obligate social parasite Polistes atrimandibularis by comparing host female-activity in parasitized and non-parasitized colonies. Host foundresses foraged more and rested less in parasitized than in non-parasitized colonies (controlling for the number of larvae in the nest, the time of day, and the day in the season). Next, we used short-term parasite removal experiments to investigate how social parasites manipulate their hosts. We found that parasitized hosts foraged more and rested less when social parasites were on the nest rather than after their removal, and we tested which kind of interactions occurred between parasites and hosts. P. atrimandibularis parasites may use mainly non-aggressive interactions (such as antennation and trophallaxis) to manipulate host activities, rather than visual, acoustic or chemical signals as other parasites do.

Development of twenty-one polymorphic microsatellite markers for the fungus-growing ant, Mycocepurus goeldii (Formicidae: Attini), using Illumina paired-end genomic sequencing

Obligate social parasites, or inquilines, exploit the colonies of free-living social species and evolved at least 80 times in ants alone. Most species of the highly specialized inquiline social parasites are rare, only known from one or very few, geographically isolated populations, and the sexual offspring of most inquiline species mates inside the maternal colony. Therefore, inquiline populations are believed to be small and genetically homogeneous due to inbreeding. To comparatively study the genetic diversity of the socially parasitic fungus-growing ant, Mycocepurus castrator, and its only known host species, Mycocepurus goeldii, and to infer the parasite’s conservation status, we developed 21 microsatellite markers for the host species, M. goeldii, and evaluated whether these markers cross-amplify in the social parasite, M. castrator. We isolated and characterized a total of 21 microsatellite loci for M. goeldii. The loci were screened for 24 individuals from geographically distant and genetically divergent populations in Brazil. The number of alleles per locus ranged from 18 to 4, the observed heterozygosity ranged from 0.25 to 0.636, and the probability of identity values ranged from 0.011 to 0.146. Preliminary analyses show that these markers cross amplify in the closely related social parasite species M. castrator. These newly developed loci provide tools for studying the genetic diversity and the evolution of social parasitism in the Mycocepurus host–parasite system.

A scientific note on Bombus (Psithyrus) insularis invasions of bumblebee nests and honeybee hives in the western USA

Bumblebees (Bombus) in the subgenus Psithyrus are obligate social parasites that usurp the nests of other bumblebees in order to reproduce. Usurpation occurs after nest establishment by the host species when, upon entry to the nest, the invading Psithyrus kills or suppresses the host queen and dominates host workers to rear her offspring, but considerable behavioral variation occurs in host–parasite interactions among members of the genus (Fisher 1988). While many Psithyrus species are known to parasitize a number of species, few of the relationships are well understood. Of the six North American Psithyrus species, most have been recorded from the nests of several host species, and it is reasonable to assume that each host species reacts differently to an invasion. In addition to usurping bumblebee nests, Plath (1927) noted that females of Psithyrus laboriosus (=Bombus citrinus (Smith)) would attempt to invade honeybee hives (Apis mellifera L.). This was noted as a “dead end,” usually resulting in the death of the invading bee. Subsequently, records of several Bombus species attempting to enter honeybee hives were made by Morse and Gary (1961), but of these records, only 1 of the 28 bumblebees found in 25 honeybee colonies was a social parasite (B. citrinus). The authors attributed these nest invasions to resource robbing and not nest usurpation. Here, we report Bombus insularis (Smith) invading the nest of two bumblebee species in the subgenus Pyrobombus, Bombus huntii Greene, and Bombus bifarius Cresson, and attempted invasions of honeybee hives at four apiaries by B. insularis. During the summer of 2012, numerous female B. insularis were observed near bumblebee nest boxes and honeybee hives in Utah, USA. Although observations from previous years were not quantified, it is uncommon to see dead B. insularis around honeybee hives; for example in 2013 at apiary 1, we found no B. insularis at three colonies during weekly inspection. The exception was in 2007 when several dead B. insularis were observed at hive entrances at apiary 1. That year, a B. insularis was observed entering a honeybee hive and was forced out within a minute. When the invader exited the hive, it had several honeybee workers attacking her, by biting her legs and tegulae; however, the parasite managed to escape and fly away. The number of invasions in 2012 by B. insularis provided an opportunity to study aspects of nest usurpation and hive invasion. We collected dead B. insularis from the ground in front of honeybee hives at four apiary sites from 12 June to 12 August (Table I). Apiary 1 was inspected weekly for dead Psithyrus in front of the hives, and apiaries 2–4 were Electronic supplementary material The online version of this article (doi:10.1007/s13592-014-0271-8) contains supplementary material, which is available to authorized users.

Evolutionary consequences of deception: Complexity and informational content of colony signature are favored by social parasitism

Abstract Nestmate recognition codes show remarkable chemical complexity, involving multiple biochemical pathways. This complexity provides the opportunity to evaluate the ecological and social conditions that favor the evolution of complex signaling. We investigated how the chemical signatures of three populations of the social paper wasp Polistes biglumis differed in terms of concentration of hydrocarbons, proportions of branched hydrocarbons and overall variation. We tested whether the variation in chemical signatures among populations could be explained by the prevalence of social parasites or whether this was just an effect of local abiotic conditions which influenced the composition of the hydrocarbon cuticular layer. We studied the chemical signature in three populations in which obligate social parasites differed in the selection pressures they imposed on host populations. Within each population, we restricted our analyses to non-parasitized hosts, to avoid potential short-term effects of parasite presence on the host chemical signatures. We found that host colonies in parasitized populations had more diverse profiles than the parasite-free population. Moreover, the overall concentration of hydrocarbons and the relative proportion of branched hydrocarbons were larger in the parasitized populations, relative to the non-parasitized one. This is to our knowledge the first evidence in favour of the hypothesis that different traits in the host chemical signatures as a whole undergo evolutionary changes resulting from directional or balancing selection imposed by social parasites. We conclude that obligate social parasites act as ‘engines of diversity’ on host chemical signatures and operate in favor of a geographic mosaic of diverging communication codes.