Parasitic Ants Research Articles

Further records of social parasitic ants in Europe and review of the Bulgarian species.

Social parasitic ants exploit the colonies of other ant species, either permanently or temporarily. The permanent parasites are amongst the rarest species of ants, although their hosts may be very common. Due to their rarity and often restricted distribution range, most of them are listed as vulnerable. Filling in the gaps in geographical and host ranges will advance our understanding of the social parasitic lifestyle's origin and evolution. This study reports the first records of the slave-makers Myrmoxenusalgerianus (Cagniant, 1968) for Europe (Italy, Sicily) and M.ravouxi (André 1896) for Albania and the inquiline Anergatesatratulus (Schenck, 1852) for Malta (Gozo). We also report new localities of Camponotusuniversitatis Forel, 1890 for Albania and Myrmoxenusgordiagini Ruzsky, 1902, M.kraussei (Emery, 1915) and Anergatesatratulus for Bulgaria. Diversity, type of parasite-host relationships, host range, distribution and conservation of social parasitic ant species in Bulgaria are discussed. Although social parasitic ants are still understudied in Bulgaria, they represent 21% of the regional ant fauna.

Prevalence and Genetic Diversity of a Microsporidian Parasite in the Black Imported Fire Ant and Its Social Parasitic Ant (Formicidae: Myrmicinae: Solenopsis) in Buenos Aires Province, Argentina.

Microsporidia are natural pathogens of arthropods and have been used as biological control against insect pests. In the United States, efforts to control the invasive Red Imported Fire Ant, Solenopsis invicta, and Black Imported Fire Ant, Solenopsis richteri, have included the use of the microsporidium, Kneallhazia solenopsae. However, there is limited information about the genetic differences among the microsporidian variants found in S. invicta and in S. richteri. In this study, we assessed the prevalence and genetic diversity of K. solenopsae in native populations of S. richteri in Argentina (South America). Additionally, we examined the social parasitic ant, Solenopsis daguerrei, which is found in some S. richteri nests, for the presence of this microsporidium. The survey of 219 S. richteri nests revealed K. solenopsae infections in all five sites analyzed, with 28 colonies (12.8%) positive for the microsporidium. Among the 180 S. daguerrei individuals collected, seven ants (3.9%) from three sites tested positive for K. solenopsae. Phylogenetic analyses of the microsporidian variants present in S. richteri and S. daguerrei based on partial small subunit ribosomal gene sequences (SSU rRNA) showed that both ant species shared the same variant, which is different from the ones found in S. invicta. Further studies are needed to determine the pathogenicity of genetically different K. solenopsae variants among Solenopsis species.

Testing optimal defence theory in a social insect: Increased risk is correlated with increased venom investment

Abstract Investment in defence may not be uniformly beneficial across an organism's lifespan. Risk, and therefore potential payoff of defence, may change with age and behaviour, but for colony‐living organisms, it may also change with colony size and reproductive stage. The acorn ant Temnothorax longispinosus uses venom to defend against socially parasitic ants that raid their nests to steal brood. We investigated the idea that T. longispinosus adjust their venom allocation in accordance with raid risk. We tested the predictions that T. longispinosus ants should produce more venom when raids are most likely to occur and during the parts of the nest reproductive cycle when the potential fitness loss per raid is highest. We also asked whether venom volume varies between nurses and foragers within a colony, which have different potential risk levels, and whether this difference increases with colony size. We found that workers had more venom in the summer, both before and during the period when raids occur, than in the fall when pupae were no longer present in nests. Workers engaging in nursing behaviours had more venom as the pupa to worker ratio in the nest increased, indicating that nurses invest more in venom as the relative number of pupae requiring defence increases. In addition, the difference in venom volume between nurses and foragers grew with colony size. These results provide observational support for the hypothesis that individuals vary their investment in venom over their colony's development in conjunction with the risk of social parasitism.

Biogeography and evolution of social parasitism in Australian Myrmecia bulldog ants revealed by phylogenomics

Studying the historical biogeography and life history transitions from eusocial colony life to social parasitism contributes to our understanding of the evolutionary mechanisms generating biodiversity in eusocial insects. The ants in the genus Myrmecia are a well-suited system for testing evolutionary hypotheses about how their species diversity was assembled through time because the genus is endemic to Australia with the single exception of the species M. apicalis inhabiting the Pacific Island of New Caledonia, and because at least one social parasite species exists in the genus. However, the evolutionary mechanisms underlying the disjunct biogeographic distribution of M. apicalis and the life history transition(s) to social parasitism remain unexplored. To study the biogeographic origin of the isolated, oceanic species M. apicalis and to reveal the origin and evolution of social parasitism in the genus, we reconstructed a comprehensive phylogeny of the ant subfamily Myrmeciinae. We utilized Ultra Conserved Elements (UCEs) as molecular markers to generate a molecular genetic dataset consisting of 2,287 loci per taxon on average for 66 out of the 93 known Myrmecia species as well as for the sister lineage Nothomyrmecia macrops and selected outgroups. Our time-calibrated phylogeny inferred that: (i) stem Myrmeciinae originated during the Paleocene ∼ 58 Ma ago; (ii) the current disjunct biogeographic distribution of M. apicalis was driven by long-distance dispersal from Australia to New Caledonia during the Miocene ∼ 14 Ma ago; (iii) the single social parasite species, M. inquilina, evolved directly from one of the two known host species, M. nigriceps, in sympatry via the intraspecific route of social parasite evolution; and (iv) 5 of the 9 previously established taxonomic species groups are non-monophyletic. We suggest minor changes to reconcile the molecular phylogenetic results with the taxonomic classification. Our study enhances our understanding of the evolution and biogeography of Australian bulldog ants, contributes to our knowledge about the evolution of social parasitism in ants, and provides a solid phylogenetic foundation for future inquiries into the biology, taxonomy, and classification of Myrmeciinae.

A caste differentiation mutant elucidates the evolution of socially parasitic ants

Most ant species have two distinct female castes-queens and workers-yet the developmental and genetic mechanisms that produce these alternative phenotypes remain poorly understood. Working with a clonal ant, we discovered a variant strain that expresses queen-like traits in individuals that would normally become workers. The variants show changes in morphology, behavior, and fitness that cause them to rely on workers in wild-type (WT) colonies for survival. Overall, they resemble the queens of many obligately parasitic ants that have evolutionarily lost the worker caste and live inside colonies of closely related hosts. The prevailing theory for the evolution of these workerless social parasites is that they evolve from reproductively isolated populations of facultative intermediates that acquire parasitic phenotypes in a stepwise fashion. However, empirical evidence for such facultative ancestors remains weak, and it is unclear how reproductive isolation could gradually arise in sympatry. In contrast, we isolated these variants just a few generations after they arose within their WT parent colony, implying that the complex phenotype reported here was induced in a single genetic step. This suggests that a single genetic module can decouple the coordinated mechanisms of caste development, allowing an obligately parasitic variant to arise directly from a free-living ancestor. Consistent with this hypothesis, the variants have lost one of the two alleles of a putative supergene that is heterozygous in WTs. These findings provide a plausible explanation for the evolution of ant social parasites and implicate new candidate molecular mechanisms for ant caste differentiation.

Cuticular Hydrocarbon Profiling by Fractionation and GC-MS in Socially Parasitic Ants.

Ants use cuticular hydrocarbon (CHC) as a semiochemical for recognizing their nestmates. For socially parasitic ants, deceiving the CHC is an important survival strategy. Profiling and quantifying CHC is a potent approach to understanding such nestmate discrimination behavior. Thus, a highly efficient, stable, and reproducible extraction method for CHC is essential for this purpose. This paper describes a method for socially parasitic ants to disguise the host species' CHC profile under laboratory conditions, as well as the extraction and measurement of CHC from ants (from a previous study). First, the artificial isotopic substance is applied to the host worker; then, the socially parasitic ant disguises the host-like CHC profile against the above host worker. Next, the CHC is extracted and fractionated from a socially parasitic ant using hexane and silica gel. After concentrating the fractionated product, this product is then used for measurement by gas chromatographymass spectrometry (GC-MS). The CHC extraction protocol described in this paper may be used for various ant species.

Multi-queen breeding is associated with the origin of inquiline social parasitism in ants

Social parasites exploit the brood care behavior of their hosts to raise their own offspring. Social parasites are common among eusocial Hymenoptera and exhibit a wide range of distinct life history traits in ants, bees, and wasps. In ants, obligate inquiline social parasites are workerless (or nearly-so) species that engage in lifelong interactions with their hosts, taking advantage of the existing host worker forces to reproduce and exploit host colonies’ resources. Inquiline social parasites are phylogenetically diverse with approximately 100 known species that evolved at least 40 times independently in ants. Importantly, ant inquilines tend to be closely related to their hosts, an observation referred to as ‘Emery’s Rule’. Polygyny, the presence of multiple egg-laying queens, was repeatedly suggested to be associated with the origin of inquiline social parasitism, either by providing the opportunity for reproductive cheating, thereby facilitating the origin of social parasite species, and/or by making polygynous species more vulnerable to social parasitism via the acceptance of additional egg-laying queens in their colonies. Although the association between host polygyny and the evolution of social parasitism has been repeatedly discussed in the literature, it has not been statistically tested in a phylogenetic framework across the ants. Here, we conduct a meta-analysis of ant social structure and social parasitism, testing for an association between polygyny and inquiline social parasitism with a phylogenetic correction for independent evolutionary events. We find an imperfect but significant over-representation of polygynous species among hosts of inquiline social parasites, suggesting that while polygyny is not required for the maintenance of inquiline social parasitism, it (or factors associated with it) may favor the origin of socially parasitic behavior. Our results are consistent with an intra-specific origin model for the evolution of inquiline social parasites by sympatric speciation but cannot exclude the alternative, inter-specific allopatric speciation model. The diversity of social parasite behaviors and host colony structures further supports the notion that inquiline social parasites evolved in parallel across unrelated ant genera in the formicoid clade via independent evolutionary pathways.

Molecular Evidence of Chemical Disguise by the Socially Parasitic Spiny Ant Polyrhachis lamellidens (Hymenoptera: Formicidae) When Invading a Host Colony

While most ant species establish a colony independently, some socially parasitic ants build the foundation of their colony by invading other ant (host) colonies and utilizing their labor forces. Many socially parasitic ants disguise their cuticular hydrocarbon (CHC) profile, which is also known as signature mixture for nestmate discrimination, when invading the host colony. Since the strategy of chemical disguise is widespread in socially parasitic ants, elucidating the mechanism of chemical disguise will promote knowledge on the evolutionary history of social parasitism. However, detailed knowledge is still lacking, as the relevant information has only originated from circumstantial evidence, which was obtained from ecological observations. In this study, we investigated the mechanism of chemical disguise in a new queen of a temporary socially parasitic spiny ant (Polyrhachis lamellidens) by measuring its CHC profile, performing a tracing assay with labeled substances, and analyzing gene expression levels. First, after rubbing behavior was observed against the host workers, the CHC profile in P. lamellidens shifted to pronounced peaks that closely resembling that of the host workers. We also observed a reduction in aggressive behaviors by the host ant against P. lamellidens after rubbing behavior was performed. In addition, P. lamellidens acquired artificially-applied labeling substances from host workers through their rubbing behaviors, while gene expression profiling showed the expression of CHC synthesis-related genes did not change during this behavior. These results suggest that P. lamellidens directly obtains host CHCs through rubbing behavior, and these host CHCs enables P. lamellidens to remain disguised during colony invasion.

Anchored phylogenomics and a revised classification of the planidial larva clade of jewel wasps (Hymenoptera: Chalcidoidea)

AbstractPlanidia are free‐living, mobile first‐instar larvae that are notable in their ability to transition across different larval stages of their host, and for completing their development on the host prepupa as ectoparasitoids, effectively acting as larval‐pupal external koinobionts. Chalcidoid taxa with a planidium form a monophyletic group, the planidial larva clade (PLC). We conducted a phylogenomic study of the PLC using anchored hybrid enrichment data. Phylogenetic analyses support the backbone relationship of PLC as: (Eutrichosomatinae, ((Philomidinae, Chrysolampinae), (Perilampinae, Eucharitidae))). Although excluded from the main analyses, the genus Jambiya, based on only 11 loci recovered, was placed as the sister of Chrysolampinae + Philomidinae or Perilampinae + Eucharitidae. Our results demonstrate that Perilampidae (Philomidinae, Chrysolampinae and Perilampinae) are paraphyletic. Divergence dating based on four node calibrations based on fossils suggests that the PLC arose approximately 111 Ma and the evolution of ant parasitism at least 64 Ma. Host associations, direct versus indirect hyperparasitism, ability to attack a host within a cocoon, soft versus hard planidial forms and mobility of the planidium were explored using a likelihood‐based ancestral state reconstruction method. A revised higher‐level classification of the PLC is proposed, with Eutrichosomatinae elevated to Eutrichosomatidae (stat. rev.), Chrysolampinae and Philomidinae placed in Chrysolampidae (stat. rev.), Perilampidae (stat. rev.) restricted to what was referred to as Perilampinae, and Eucharitidae maintained with four subfamilies, with Akapalinae (unknown biology) as sister group to the core Eucharitidae, all of which are ant parasitoids. Jambiya is treated as an incertae sedis taxon within the planidial clade.

The real deal: the ant species, Pheidole sauberi (Hymenoptera: Formicidae), first description of the queen and first record of a mermithergate in the Philippines

The occurrence of mermithism in ants is reported for the first time in the Philippines. The mermithergate worker and previously undescribed dealate queen of Pheidole sauberi are described. The mermithergate worker is intermediate in size between the major and minor workers and pale yellow in color, in contrast to the brown healthy workers, and has a much larger gaster than either uninfected subcaste. Colony demographics and nest ecology are also reported. This find offers an opportunity for interdisciplinary research on ant parasitism.

Ectoparasitic fungi of Myrmica ants alter the success of parasitic butterflies

Exploitation of organisms by multiple parasite species is common in nature, but interactions among parasites have rarely been studied. Myrmica ants are rich in parasites. Among others, the ectoparasitic Rickia wasmannii fungus and the parasitic caterpillars of myrmecophilous Phengaris butterflies often infect the same Myrmica colonies. In this study, we examined the effects of R. wasmannii on the adoption, long-term development, and survival of P. alcon. In laboratory conditions, caterpillars introduced into nests of Myrmica scabrinodis uninfected with R. wasmannii survived significantly longer compared to caterpillars introduced into infected nests. In the field, joint infection was less common than expected if both parasites exploited M. scabrinodis colonies independently. Pre-pupal caterpillars of P. alcon were somewhat larger in nests infected with R. wasmannii than those found in uninfected nests. Based on these results it seems that R. wasmannii infection of M. scabrinodis affects the survival and development of P. alcon caterpillars, suggesting competition between these two ant parasites.

The evolution of social parasitism in Formica ants revealed by a global phylogeny

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica, obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

The Inquiline Ant Myrmica karavajevi Uses Both Chemical and Vibroacoustic Deception Mechanisms to Integrate into Its Host Colonies.

Simple SummaryAlthough fiercely defended by workers, ant societies can be infiltrated by social parasites that exploit the whole colony and its resources, instead of taking advantage of a single organism. Among them, we studied Myrmica karavajevi, a rare ant species in which the worker caste does not exist, and queens live as “inquilines” within colonies of another ant species, commonly Myrmica scabrinodis. Parasite queens entirely depend on host worker labour. They have evolved many adaptations to be admitted and integrate as members of the host ant society. Indeed, we found that, even at the pupal stage, the parasite is treated as a valuable item in the colony hierarchy, as it is rescued ahead of the colony’s own brood. Moreover, we discovered that M. karavajevi adult queens use two strategies to live undisturbed in the host nest. The parasite smells like the host queens by possessing specific odours and produces sounds similar to those emitted by M. scabrinodis ants, particularly by queens. Through these kinds of mimicking, M. karavajevi advances its rank towards the highest attainable position in the colony’s hierarchy. M. karavajevi is an outstanding example of multimodal deception, which needs a combined behavioural and molecular approach to be fully unravelled.Social parasitism represents a particular type of agonistic interaction in which a parasite exploits an entire society instead of a single organism. One fascinating form of social parasitism in ants is the “inquilinism”, in which a typically worker-less parasitic queen coexists with the resident queen in the host colony and produces sexual offspring. To bypass the recognition system of host colonies, inquilines have evolved a repertoire of deceiving strategies. We tested the level of integration of the inquiline Myrmica karavajevi within the host colonies of M. scabrinodis and we investigated the mechanisms of chemical and vibroacoustic deception used by the parasite. M. karavajevi is integrated into the ant colony to such an extent that, in rescue experiments, the parasite pupae were saved prior to the host’s brood. M. karavajevi gynes perfectly imitated the cuticular hydrocarbon profiles of M. scabrinodis queens and the parasite vibroacoustic signals resembled those emitted by the host queens eliciting the same levels of attention in the host workers during playback experiments. Our results suggest that M. karavajevi has evolved ultimate deception strategies to reach the highest social status in the colony hierarchy, encouraging the use of a combined molecular and behavioural approach when studying host–parasite interactions.

Mixed-colony records together with nest densities and gyne morphology suggest temporary social parasitism in Tetramorium (Hymenoptera: Formicidae)

Two types of permanent social parasitism, dulosis and inquilinism, are well known in the ant genus Tetramorium Mayr, 1855. In contrast, temporary social parasitism has never been reported for these ants. A recently detected mixed colony of Tetramorium immigrans Santschi, 1927 and the putative social parasite Tetramorium aspina Wagner et al., 2018 make it thinkable that additional social parasites exist in the genus with more than 500 species known. Here, we extended our research to species putatively related evolutionarily to T. aspina, and detected two mixed colonies of Tetramorium moravicum Novák & Sadil, 1941 and Tetramorium ferox Ruzsky, 1903. The hypothesis that the latter is a parasite of the former is tested via three lines of indirect evidence using literature and self-collected data: 1) The distributional area of T. ferox is congruent with or a part of that of T. moravicum; 2) Nest densities of T. ferox are lower than those of independently founding Tetramorium species; 3) T.-ferox-complex gynes show a morphology fitting the parasitic syndrome. The alternative hypothesis to social parasitism is that T. ferox is free-living. Line 1 does not fully support the hypothesis of social parasitism but requires multiple host species as extra assumption to justify the hypothesis. In contrast, the two other lines of evidence support the hypothesis: The known maximum nest densities of T. ferox are significantly lower than in independently founding species (Line 2). Gynes of the T. ferox complex are smaller, have a deeper clypeal excision, smaller mesosoma, wider waist, and smaller gaster than independently founding species (Line 3). Moreover, a stronger positive allometry of waist width in species of the T. ferox complex indicates an adaptive value of this specific structure. We consider obligatory temporary social parasitism in the T. ferox complex as the most likely colony-foundation strategy. Temporary social parasitism might represent the evolutionary link between independent and dulotic species, and our findings may foster better understanding the evolutionary pathway of social parasitism in ants.

Differential parasitism by four species of phorid flies when attacking three worker castes of the leaf-cutting ant Atta laevigata (Smith, 1858).

Certain species of parasitic flies belonging to the Phoridae are known to attack Atta spp. workers foraging along trails, near nest openings used by the ants to supply the colony with plant material, and in the areas where the ants are actively cutting plant material. However, there have been no previous studies of phorid parasitism of non-foraging worker ants, for example excavators and soldiers. Excavators can be found on the surface around specialized nest openings, carrying and dumping soil on characteristic mounds. Soldiers can be found on the trails protecting foragers or guarding the different types of nest openings. The current study was performed to investigate the differential parasitism rates of Atta laevigata (Smith, 1858) worker castes by four species of phorids. Ants of all castes on trails and at nest entrances were collect from 18 mature colonies in the field. A total of 21,254 ants were collected from trails and 14,649 collected from the mounds of loose soil near nest openings. The captured workers were maintained under controlled laboratory conditions to evaluate the rate of parasitism. Of the ants collected from trails, 1,112 (5.23%) were found to have been parasitized, of which 1,102 were foragers and only 10 were soldiers. Of the ants collected from the soil mounds near the nest openings, only 27 (0.18%) were found to have been parasitized, of those 25 were excavators and 2 were soldiers. When evaluating parasitism of ants on the trails, 46.2% were attacked by Apocephalus attophilus Borgmeier, 1928, 22.6% by Myrmosicarius grandicornis Borgmeier, 1928, 16.6% by Eibesfeldtphora erthali (Brown, 2001) and 14.6% by Apocephalus vicosae Disney, 2000. Only two species of phorid, M. grandicornis and E. erthali, were observed parasitizing excavators, whilst only E. erthali parasitized soldiers. This is the first time that Atta spp. excavators and soldiers have been shown to be parasitized by phorids. The low rates of parasitism and specificity of certain phorid species for excavators and soldiers is discussed in relation to the behavioral interactions of hosts and their parasitoids, as well as the relationship between host and parasitoid size.

Les périodes d’essaimage des fourmis parasites du sous-genre Chthonolasius observées dans la région Hauts-de-France (Hymenoptera : Formicidae : Formicinae)

Swarming periods of parasitic ants from the subgenus Chthonolasius observed in the Hauts-de-France region (Hymenoptera: Formicidae: Formicinae). - Swarming periods of parasitic ants from the subgenus Chthonolasius are studied in Northern France. This work, carried out between 2014 and 2020, improves our understanding of their strategy for parasitising host species. The role of insect traps for the study of this group of insects is underlined, especially the light traps which seems to be the most effective technique for detecting individuals belonging to this subgenus. The data collected also makes possible to question the patrimonial value of these species.

Evolutionary history of inquiline social parasitism in Plagiolepis ants

Social parasitism, i.e. the parasitic dependence of a social species on another free-living social species, is one of the most intriguing phenomena in social insects. It has evolved to various levels, the most extreme form being inquiline social parasites which have lost the worker caste, and produce only male and female sexual offspring that are reared by the host worker force. The inquiline syndrome has been reported in 4 species within the ant genus Plagiolepis, in Europe. Whether inquiline social parasitism evolved once or multiple times within the genus remains however unknown. To address this question, we generated data for 5 inquiline social parasites – 3 species previously described and 2 unidentified species – and their free-living hosts from Europe, and we inferred their phylogenetic relationships. We tested Emery’s rule, which predicts that inquiline social parasites and their hosts are close relatives. Our results show that inquiline parasitism evolved independently at least 5 times in the genus. Furthermore, we found that all inquilines were associated with one of the descendants of their most related free-living species, suggesting sympatric speciation is the main process leading to the emergence of the parasitic species, consistent with the stricter version of Emery’s rule.

Social parasite distancing: RADseq reveals high inbreeding in the social parasite Microdon myrmicae but low philopatry for host ant nest

The hoverfly Microdon myrmicae is a rare and extremely localised social parasite of Myrmica ants, only occurring around wet grassland. Dispersal, location of the host, and oviposition are crucial steps in the life of ant parasites but are poorly known due to the challenge of studying such rare species. Using genome‐wide loci obtained by RADseq, we investigated the genetic structure and relatedness of Mi. myrmicae larvae and its ant host, collected from three localities in South West England, and inferred biological and behavioural traits. We found that: (a) Mi. myrmicae larvae show high inbreeding levels and severe heterozygosity deficiency, as an expression of the small population size that favours the mating between siblings or half‐siblings; (b) Mi. myrmicae adults can disperse for many kilometres, spreading much more than it is reported for its sibling species, Microdon mutabilis; (c) a single female lays small egg bunches in different ant colonies, sometimes spanning substantial distances (bet‐hedging strategy); in parallel, a single ant nest can harbour eggs from different Microdon females; (d) preliminary evidence suggest that contrary to Mi. mutabilis, host colony choice seems not to depend on the number of queens residing in a single colony. These results overall strongly deviate from what previously found for Mi. mutabilis, whose females oviposit in the natal nest generation after generation. We argue that such different ecological traits and parasitic strategies between closely related species are mainly ascribable to the different selective pressure on the two ant hosts.

Evolution: Shape-Shifting Social Parasites

Ants exploit differences in body surface chemistry to distinguish nestmates from colony intruders. Socially parasitic ants in Madagascar have convergently evolved morphological similarities to host worker anatomy, implying that body shape may also be surveilled. Studies of tactile behaviors in ant societies are now needed.

Socially Parasitic Ants Evolve a Mosaic of Host-Matching and Parasitic Morphological Traits

A basic expectation of evolution by natural selection is that species morphologies will adapt to their ecological niche. In social organisms, this may include selective pressure from the social environment. Many non-ant parasites of ant colonies are known to mimic the morphology of their host species, often in striking fashion [1, 2], indicating there is selection on parasite morphology to match the host (Batesian and/or Wasmannian mimicry [3]). However, ants that parasitize other ant societies are usually closely related to their hosts (Emery's rule) [4-8] and expected to be similar due to common ancestry, making any kind of mimicry difficult to detect [9]. Here, we investigate the diversification of the hyperdiverse ant genus Pheidole in Madagascar, including the evolution of 13 putative social parasite species within a broader radiation of over 100 ant species on the island. We find that the parasitic species are monophyletic and that their associated hosts are spread across the Malagasy Pheidole radiation. This provides an opportunity to test for selection on morphological similarity and divergence between parasites and hosts. Using X-ray microtomography and both linear measurements and three-dimensional (3D) geometric morphometrics, we show that ant social parasite worker morphologies feature a mix of "host-matching" and "parasitic" traits, where the former converge on the host phenotype and the latter diverge from typical Pheidole phenotypes to match a common parasitic syndrome. This finding highlights the role of social context in shaping the evolution of phenotypes and raises questions about the role of morphological sensing in nestmate recognition.