Genomic basis of adaptation to climate and parasite prevalence and the importance of odorant perception in the ant Temnothorax longispinosus.

A co-evolutionary arms race ensues when parasites exhibit exploitative behaviour, which prompts adaptations in their hosts, in turn triggering counter-adaptations by the parasites. To unravel the genomic basis of this coevolution from the host's perspective, we collected ants of the host species Temnothorax longispinosus, parasitized by the social parasite Temnothorax americanus, from 10 populations in the northeastern United States exhibiting varying levels of parasite prevalence and living under different climatic conditions. We conducted a genome-wide association study (GWAS) to identify single nucleotide polymorphisms (SNPs) associated with both prevalence and climate. Our investigation highlighted a multitude of candidate SNPs associated with parasite prevalence, particularly in genes responsible for sensory perception of smell including odorant receptor genes. We further focused on population-specific compositions of cuticular hydrocarbons, a complex trait important for signalling, communication and protection against desiccation. The relative abundances of n-alkanes were correlated with climate, while there was only a trend between parasite prevalence and the relative abundances of known recognition cues. Furthermore, we identified candidate genes likely involved in the synthesis and recognition of specific hydrocarbons. In addition, we analysed the population-level gene expression in the antennae, the primary organ for odorant reception, and established a strong correlation with parasite prevalence. Our comprehensive study highlights the intricate genomic patterns forged by the interplay of diverse selection factors and how these are manifested in the expression of various phenotypes.

With the dead under the mat: the zombie ant extended phenotype under a new perspective.

Some parasitic fungi can increase fitness by modifying the behavior of their hosts. These behaviors are known as extended phenotypes because they favor parasitic gene propagation. Here, we studied three lineages of Ophiocordyceps, a fungus that infects ants, altering their conduct before death. According to fungal strategy, ants may die in leaf litter, with entwined legs in branches, under the moss mat, or biting plant tissue. It is critical for parasites that the corpses stay at these places because Ophiocordyceps exhibit iteroparity, possibly releasing spores in multiple life cycles. Thus, we assumed substrate cadaver permanence as a fungi reproductive proxy and corpse height as a proxy of cadaver removal. We hypothesize that biting vegetation and dying in higher places may increase the permanence of ant corpses while avoiding possible corpse predation on the forest floor. We monitored over a year more than 4000 zombie ants in approximately 15 km2 of undisturbed tropical forest in central Amazonia. Our results show a longer permanence of corpses with increasing ground height, suggesting that the parasites may have better chances of releasing spores and infecting new hosts at these places. We found that the zombie ants that last longer on the substrate die under the moss mat in tree trunks, not necessarily biting vegetation. The biting behavior appears to be the most derived and complex mechanism among Ophiocordyceps syndromes. Our results put these findings under a new perspective, proposing that seemingly less complex behavioral changes are ecologically equivalent and adaptative for other parasite lineages.

Clonemate cotransmission supports a role for kin selection in a puppeteer parasite.

Host manipulation by parasites is a fascinating evolutionary outcome, but adaptive scenarios that often accompany even iconic examples in this popular field of study are speculative. Kin selection has been invoked as a means of explaining the evolution of an altruistic-based, host-manipulating behavior caused by larvae of the lancet fluke Dicrocoelium dendriticum in ants. Specifically, cotransmission of larval clonemates from a snail first host to an ant second host is presumed to lead to a puppeteer parasite in the ant's brain that has clonemates in the ant abdomen. Clonal relatedness between the actor (brain fluke) and recipients (abdomen flukes) enables kin selection of the parasite's host-manipulating trait, which facilitates transmission of the recipients to the final host. However, the hypothesis that asexual reproduction in the snail leads to a high abundance of clonemates in the same ant is untested. Clonal relationships between the manipulator in the brain and the nonmanipulators in the abdomen are also untested. We provide empirical data on the lancet fluke's clonal diversity within its ant host. In stark contrast to other trematodes, which do not exhibit the same host-manipulating behavioral trait, the lancet fluke has a high abundance of clonemates. Moreover, our data support existing theory that indicates that the altruistic behavior can evolve even in the presence of multiple clones within the same ant host. Importantly, our analyses conclusively show clonemate cotransmission into ants, and, as such, we find support for kin selection to drive the evolution and maintenance of this iconic host manipulation.

Hijacking time: How Ophiocordyceps fungi could be using ant host clocks to manipulate behavior.

Ophiocordyceps fungi manipulate ant behaviour as a transmission strategy. Conspicuous changes in the daily timing of disease phenotypes suggest that Ophiocordyceps and other manipulators could be hijacking the host clock. We discuss the available data that support the notion that Ophiocordyceps fungi could be hijacking ant host clocks and consider how altering daily behavioural rhythms could benefit the fungal infection cycle. By reviewing time-course transcriptomics data for the parasite and the host, we argue that Ophiocordyceps has a light-entrainable clock that might drive daily expression of candidate manipulation genes. Moreover, ant rhythms are seemingly highly plastic and involved in behavioural division of labour, which could make them susceptible to parasite hijacking. To provisionally test whether the expression of ant behavioural plasticity and rhythmicity genes could be affected by fungal manipulation, we performed a gene co-expression network analysis on ant time-course data and linked it to available behavioural manipulation data. We found that behavioural plasticity genes reside in the same modules as those affected during fungal manipulation. These modules showed significant connectivity with rhythmic gene modules, suggesting that Ophiocordyceps could be indirectly affecting the expression of those genes as well.

Canine serological survey and dog culling ant its relationship with human visceral leishmaniasis in an endemic urban area.

BACKGROUND: Visceral leishmaniasis is an important but neglected disease that is spreading and is highly lethal when left untreated. This study sought to measure the Leishmania infantum seroprevalence in dogs, the coverage of its control activities (identification of the canine reservoir by serological survey, dog culling and insecticide spraying) and to evaluate its relationship with the occurrence of the disease in humans in the municipalities of Araçatuba and Birigui, state of São Paulo, Brazil. METHODS: Information from 2006 to 2015 was georeferenced for each municipality and modeling was performed for the two municipalities together. To do this, latent Gaussian Bayesian models with the incorporation of a spatio-temporal structure and Poisson distribution were used. The Besag-York-Mollie models were applied for random spatial effects, as also were autoregressive models of order 1 for random temporal effects. The modeling was performed using the INLA (Integrated Nested Laplace Approximations) deterministic approach, considering both the numbers of cases as well as the coverage paired year by year and lagged at one and two years. RESULTS: Control activity coverage was observed to be generally low. The behavior of the temporal tendency in the human disease presented distinct patterns in the two municipalities, however, in both the tendency was to decline. The canine serological survey presented as a protective factor only in the two-year lag model. CONCLUSIONS: The canine serological coverage, even at low intensity, carried out jointly with the culling of the positive dogs, suggested a decreasing effect on the occurrence of the disease in humans, whose effects would be seen two years after it was carried out.

The possible role of ant larvae in the defence against social parasites.

Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca, consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.

Chemical Deception and Structural Adaptation in Microdon (Diptera, Syrphidae, Microdontinae), a Genus of Hoverflies Parasitic on Social Insects.

Various organisms, especially arthropods, are able to live as parasites in ant nests and to prey upon ant broods without eliciting any aggressive behaviour in the hosts. Understanding how these intruders are able to break the ants' communication codes in their favour represents a challenging and intriguing evolutionary question. We studied the chemical strategies of three European hoverfly species, Microdon mutabilis (parasitic on Formica cunicularia), M. analis (parasitic on Lasius emarginatus) and M. devius (parasitic on L. distinguendus). The peculiar slug-like larvae of these three species live inside ant nests feeding upon their broods. Gas chromatography-mass spectrometry analyses show that: 1) these parasites mimic the host brood rather than the ant workers, although each differs distinctly in the extent of chemical mimicry; 2) isolation experiments indicate that after 14 days the responsible cuticular hydrocarbons (CHCs) are not passively acquired but synthesized by the fly larvae. Additionally, Microdon larvae show an array of protective structural features, such as a thick and multi-layered cuticle, retractable head, dome-shaped tergum and a flat and strongly adhesive "foot" (sternum). This combination of protective chemical and structural features represents a successful key innovation by Microdon species, and one that may facilitate host switching. The results of a preliminary adoption analysis confirm that Microdon larvae of at least some species can readily be accepted by different species of ants.

Parasitism by Phorids on Leaf Cutter Ants Atta sexdens (Linnaeus, 1758) (Hymenoptera: Formicidae) in Natural and Agricultural Environments.

The leaf cutter ant Atta sexdens (L.) (Hymenoptera:Formicidae) causes huge economic losses to agriculture in the Neotropics. In natural environments, parasitic flies of the Phoridae family are natural enemies of leaf cutter ants. Habitat modification is considered one of the main causes of species decline. In this study, we compare the occurrence of parasitic phorids on A. sexdens and the parasitism that they cause on colonies located in agricultural and natural habitats. Phorid flies were collected from trails, nest entrances, and cutting sites when they were hovering over workers of A. sexdens nests from natural vegetation, farmland, and Eucalyptus plantation areas. Simultaneously, workers from A. sexdens nests were collected from these environments, and the parasitism rates of phorids were determined. Ants were parasitized by Apocephalus attophilus, A. vicosae, Eibesfeldtphora bragancai, E. tonhascai, and Myrmosicarius grandicornis. The highest parasitism rate (3.54 ± 0.49%) was registered for nests from the Eucalyptus plantations. The rate of parasitism of nest from natural vegetation was 2.42 ± 0.40% and in the farmland was 1.91 ± 0.39%. The parasitism of each phorid genus varied according to habitat and month. Apocephalus attophilus had the highest parasitism in the three habitats and displayed biological characteristics that give it great potential as a biological control agent for A. sexdens. Eibesfeldtphora spp. had higher parasitism in a natural environment and M. grandicornis in agricultural environments. Apocephalus attophilus and M. grandicornis seemed able to occur in a wide variety of habitats that their hosts occupy, but the rate of parasitism by Eibesfeldtphora spp. was significantly lower in agricultural environments.

Pseudacteon Phorid Flies: Host Specificity and Impacts on Solenopsis Fire Ants.

Human commerce has resulted in the spread of the imported fire ants, Solenopsis species, worldwide. Six species of parasitic Pseudacteon phorid flies that are highly host specific to the Solenopsis saevissima complex of Solenopsis fire ants have been successfully released in the southern United States. The presence of Pseudacteon phorid flies, in addition to having direct mortality effects on their host ants, modifies foraging behavior and disrupts interspecific competition between host species and other ant species in the community. Fire ant workers have evolved effective methods to cope with parasitism pressure, which may relieve population-level impacts of introduced phorid flies. This review focuses on the mechanisms underlying host location, host preference, and host-size selection of Pseudacteon phorid flies and highlights their direct and indirect effects on fire ant populations. Knowledge gained from parasitoid-ant interactions will enhance use of natural enemies as biological control agents for invasive social insects.

Effects of Host Interspecific Interaction in the Maculinea-Myrmica Parasite-Host System.

A model of interspecific host competition in a system with one parasite (butterfly-Maculinea) and multiple potential hosts (ants-Myrmica) is presented. Results indicate that host interspecific competition increases the occurrence of multiple host behaviour in Maculinea natural populations but decreases the ability of the parasite populations to adapt to the most abundant host species. These qualitative predictions were compared with data on host specificity, with good agreement. Analysis of the data also indicates that Maculinea teleius and Maculinea arion respond differently to changes in relative host abundances. Maculinea teleius shows a larger fraction of sites where it displays multiple host behaviour and a larger fraction of sites where the niches of the hosts overlap. In some instances, Maculinea teleius is adapted to Myrmica hosts that are present in lower frequencies. Maculinea arion is locally more host-specific and occurs at sites where host interspecific competition is unlikely and is more frequently adapted to the most abundant host species.

Diversity and abundance of entomopathogenic fungi at ant colonies.

The purpose of this study was to identify whether entomopathogenic fungi in the genera Metarhizium and Beauveria were found at ant nests. These fungi have been used in studies of ant social immunity, however experimental conditions used may not normally be representative of that found within ant colonies. The presence of insect pathogenic fungi including Metarhizium and Beauveria was assessed in soils at 22 ant nests in Ontario, Canada. Soil samples were plated onto selective agar, fungi were isolated and DNA extracted and the fungi identified by amplifying the internal transcribed spacer region (ITS) and comparing sequences to those found in GenBank. We found that Metarhizium species were found in soils in and around most ant nests. Concentrations of Metarhizium in the soil were not influenced by the presence of ant nests suggesting co-existence rather than avoidance or seeking behaviour. Thus, Metarhizium appears to be a good pathogen to study ant-fungal interactions. Beauveria on the other hand, was not found in any of the samples indicating a decreased likelihood that ants encounter this pathogen. Other fungi found at relatively high concentrations at ant nests include Pochonia and Purpureocillium species, both recognized as nematode pathogens.

Species-specific genes under selection characterize the co-evolution of slavemaker and host lifestyles.

BACKGROUND: The transition to a parasitic lifestyle entails comprehensive changes to the selective regime. In parasites, genes encoding for traits that facilitate host detection, exploitation and transmission should be under selection. Slavemaking ants are social parasites that exploit the altruistic behaviour of their hosts by stealing heterospecific host brood during raids, which afterwards serve as slaves in slavemaker nests. Here we search for evidence of selection in the transcriptomes of three slavemaker species and three closely related hosts. We expected selection on genes underlying recognition and raiding or defense behaviour. Analyses of selective forces in species with a slavemaker or host lifestyle allowed investigation into whether or not repeated instances of slavemaker evolution share the same genetic basis. To investigate the genetic basis of host-slavemaker co-evolution, we created orthologous clusters from transcriptome sequences of six Temnothorax ant species - three slavemakers and three hosts - to identify genes with signatures of selection. We further tested for functional enrichment in selected genes from slavemakers and hosts respectively and investigated which pathways the according genes belong to. RESULTS: Our phylogenetic analysis, based on more than 5000 ortholog sequences, revealed sister species status for two slavemakers as well as two hosts, contradicting a previous phylogeny based on mtDNA. We identified 309 genes with signs of positive selection on branches leading to slavemakers and 161 leading to hosts. Among these were genes potentially involved in cuticular hydrocarbon synthesis, thus species recognition, and circadian clock functionality possibly explaining the different activity patterns of slavemakers and hosts. There was little overlap of genes with signatures of positive selection among species, which are involved in numerous different functions and different pathways. CONCLUSIONS: We identified different genes, functions and pathways under positive selection in each species. These results point to species-specific adaptations rather than convergent trajectories during the evolution of the slavemaker and host lifestyles suggesting that the evolution of parasitism, even in closely related species, may be achieved in diverse ways.

Artificial selection on ant female caste ratio uncovers a link between female-biased sex ratios and infection by Wolbachia endosymbionts.

Social insect sex and caste ratios are well-studied targets of evolutionary conflicts, but the heritable factors affecting these traits remain unknown. To elucidate these factors, we carried out a short-term artificial selection study on female caste ratio in the ant Monomorium pharaonis. Across three generations of bidirectional selection, we observed no response for caste ratio, but sex ratios rapidly became more female-biased in the two replicate high selection lines and less female-biased in the two replicate low selection lines. We hypothesized that this rapid divergence for sex ratio was caused by changes in the frequency of infection by the heritable bacterial endosymbiont Wolbachia, because the initial breeding stock varied for Wolbachia infection, and Wolbachia is known to cause female-biased sex ratios in other insects. Consistent with this hypothesis, the proportions of Wolbachia-infected colonies in the selection lines changed rapidly, mirroring the sex ratio changes. Moreover, the estimated effect of Wolbachia on sex ratio (~13% female bias) was similar in colonies before and during artificial selection, indicating that this Wolbachia effect is likely independent of the effects of artificial selection on other heritable factors. Our study provides evidence for the first case of endosymbiont sex ratio manipulation in a social insect.

Arthropods Associate with their Red Wood ant Host without Matching Nestmate Recognition Cues.

Social insect colonies provide a valuable resource that attracts and offers shelter to a large community of arthropods. Previous research has suggested that many specialist parasites of social insects chemically mimic their host in order to evade aggression. In the present study, we carry out a systematic study to test how common such chemical deception is across a group of 22 arthropods that are associated with red wood ants (Formica rufa group). In contrast to the examples of chemical mimicry documented in some highly specialized parasites in previous studies, we find that most of the rather unspecialized red wood ant associates surveyed did not use mimicry of the cuticular hydrocarbon recognition cues to evade host detection. Instead, we found that myrmecophiles with lower cuticular hydrocarbon concentrations provoked less host aggression. Therefore, some myrmecophiles with low hydrocarbon concentrations appear to evade host detection via a strategy known as chemical insignificance. Others showed no chemical disguise at all and, instead, relied on behavioral adaptations such as particular defense or evasion tactics, in order to evade host aggression. Overall, this study indicates that unspecialized myrmecophiles do not require the matching of host recognition cues and advanced strategies of chemical mimicry, but can integrate in a hostile ant nest via either chemical insignificance or specific behavioral adaptations.

What are the Mechanisms Behind a Parasite-Induced Decline in Nestmate Recognition in Ants?

Social insects have developed sophisticated recognition skills to defend their nests against intruders. They do this by aggressively discriminating against non-nestmates with deviant cuticular hydrocarbon (CHC) signatures. Studying nestmate recognition can be challenging as individual insects do not only vary in their discriminatory abilities, but also in their motivation to behave aggressively. To disentangle the influence of signaling and behavioral motivation on nestmate recognition, we investigated the ant Temnothorax nylanderi, where the presence of tapeworm-infected nestmates leads to reduced nestmate recognition among uninfected workers. The parasite-induced decline in nestmate recognition could be caused by higher intra-colonial cue diversity as tapeworm-infected workers are known to exhibit a modified hydrocarbon signature. This in turn may broaden the neuronal template of their nestmates, leading to a higher tolerance towards alien conspecifics. To test this hypothesis, we exchanged infected ants between colonies and analyzed their impact on CHC profiles of uninfected workers. We demonstrate that despite frequent grooming, which should promote the transfer of recognition cues, CHC profiles of uninfected workers neither changed in the presence of tapeworm-infected ants, nor did it increase cue diversity among uninfected nestmates within or between colonies. However, CHC profiles were systematically affected by the removal of nestmates and addition of non-nestmates, independently from the ants' infection status. For example, when non-nestmates were present workers expressed more dimethyl alkanes and higher overall CHC quantities, possibly to achieve a better distinction from non-nestmates. Workers showed clear task-specific profiles with tapeworm-infected workers resembling more closely young nurses than older foragers. Our results show that the parasite-induced decline in nestmate recognition is not due to increased recognition cue diversity or altered CHC profiles of uninfected workers, but behavioral changes might explain tolerance towards intruders.

Reproductive ecology of phorid parasitoids in relation to the head size of leaf-cutting ants Atta sexdens Forel.

The leaf-cutting ant Atta sexdens Forel (Hymenoptera: Formicidae) is one of the most damaging agricultural pests in the Neotropics. Management strategies predominantly rely on the use of general insecticides. What is needed are more species-specific and environmentally friendly options. Parasitioids such as phorid flies (Diptera: Phoridae) may be one such option, but a greater understanding of the ecology of the flies and their ant hosts is essential to devise biological control strategies. Here we report parasitism rates, ant host size, parasitoid abundance per host and resultant sex ratios of two phorid species Apocephalus attophilus Borgmeier and Eibesfeldtphora tonhascai Brown parasitizing A.sexdens. The two species achieved parasitism rates of 1.48 and 1.46%, respectively and the pupal period was 14.7 ± 1.1 days and 22.1 ± 2.8 days, respectively. There was no significant difference between the head capsule width of ants parasitized by either A. attophilus or E. tonhascai. Likewise, there was no significant effect between the head capsule width of parasitized and unparasitized ants for both species. A significant positive correlation was found between the head capsule width of the parasitized ants and the number of adult parasitoids A. attophilus emerged. Ants parasitized by E. tonhascai survived significantly longer than those parasitized by A. attophilus. There was no significant effect of ant head width on the sex ratio of the offspring of either parasitoid species and no significant difference in the sex ratio (male: female) of their offspring. In summary, these data addressed here are important steps when considering natural enemies for biological control. Studying survival of the parasitized ants, parasitoid offspring sex ratio and host size preference allows for a better understanding of ant natural biological control in the field and can help in rearing of A. attophilus and E. tonhascai in laboratory.

Studying the Complex Communities of Ants and Their Symbionts Using Ecological Network Analysis.

Ant colonies provide well-protected and resource-rich environments for a plethora of symbionts. Historically, most studies of ants and their symbionts have had a narrow taxonomic scope, often focusing on a single ant or symbiont species. Here we discuss the prospects of studying these assemblies in a community ecology context using the framework of ecological network analysis. We introduce three basic network metrics that we consider particularly relevant for improving our knowledge of ant-symbiont communities: interaction specificity, network modularity, and phylogenetic signal. We then discuss army ant symbionts as examples of large and primarily parasitic communities, and symbiotic sternorrhynchans as examples of generally smaller and primarily mutualistic communities in the context of these network analyses. We argue that this approach will provide new and complementary insights into the evolutionary and ecological dynamics between ants and their many associates, and will facilitate comparisons across different ant-symbiont assemblages as well as across different types of ecological networks.

Do well-integrated species of an inquiline community have a lower brood predation tendency? A test using red wood ant myrmecophiles.

BACKGROUND: A host infected with multiple parasitic species provides a unique system to test evolutionary and ecological hypotheses. Different parasitic species associated with a single host are expected to occupy different niches. This niche specialization can evolve from intraguild competition among parasites. However, niche specialization can also be structured directly by the host when its defence strategy depends on the parasite's potential impact. Then it can be expected that species with low or no tendency to prey on host brood will elicit less aggression than severe brood parasitic species and will be able to integrate better in the host system. We examined this hypothesis in a large community of symbionts associated with European red wood ants (Formica rufa group) by testing the association between 1) level of symbiont integration (i.e. presence in dense brood chambers vs. less populated chambers without brood) 2) level of ant aggression towards the symbiont 3) brood predation tendency of the symbiont. RESULTS: Symbionts differed vastly in integration level and we demonstrated for the first time that relatively unspecialized ant symbionts or myrmecophiles occur preferentially in brood chambers. Based on their integration level, we categorize the tested myrmecophiles into three categories: 1) species attracted to the dense brood chambers 2) species rarely or never present in the brood chambers 3) species randomly distributed throughout the nest. The associates varied greatly in brood predation tendency and in aggression elicited. However, we did not find a correlation for the whole myrmecophile community between a) brood predation tendency and host's aggression b) integration level and host's aggression c) integration level and brood predation tendency. CONCLUSIONS: Our results indicate that red wood ants did not act more hostile towards species that have a high tendency to prey on brood compared to species that are less likely or do not prey on brood. We show that potentially harmful parasites can penetrate into the deepest parts of a social insect fortress. We discuss these seemingly paradoxical findings in relation to models on coevolution and evolutionary arms races and list factors which can make the presence of potentially harmful parasites within the brood chambers evolutionary stable.

Dead ant walking: a myrmecophilous beetle predator uses parasitoid host location cues to selectively prey on parasitized ants.

Myrmecophiles (i.e. organisms that associate with ants) use a variety of ecological niches and employ different strategies to survive encounters with ants. Because ants are typically excellent defenders, myrmecophiles may choose moments of weakness to take advantage of their ant associates. This hypothesis was studied in the rove beetle, Myrmedonota xipe, which associates with Azteca sericeasur ants in the presence of parasitoid flies. A combination of laboratory and field experiments show that M. xipe beetles selectively locate and prey upon parasitized ants. These parasitized ants are less aggressive towards beetles than healthy ants, allowing beetles to eat the parasitized ants alive without interruption. Moreover, behavioural assays and chemical analysis reveal that M. xipe are attracted to the ant's alarm pheromone, the same secretion used by the phorid fly parasitoids in host location. This strategy allows beetles access to an abundant but otherwise inaccessible resource, as A. sericeasur ants are typically highly aggressive. These results are the first, to our knowledge, to demonstrate a predator sharing cues with a parasitoid to gain access to an otherwise unavailable prey item. Furthermore, this work highlights the importance of studying ant-myrmecophile interactions beyond just their pairwise context.

Fitness costs of worker specialization for ant societies.

Division of labour is of fundamental importance for the success of societies, yet little is known about how individual specialization affects the fitness of the group as a whole. While specialized workers may be more efficient in the tasks they perform than generalists, they may also lack the flexibility to respond to rapid shifts in task needs. Such rigidity could impose fitness costs when societies face dynamic and unpredictable events, such as an attack by socially parasitic slavemakers. Here, we experimentally assess the colony-level fitness consequences of behavioural specialization in Temnothorax longispinosus ants that are attacked by the slavemaker ant T. americanus. We manipulated the social organization of 102 T. longispinosus colonies, based on the behavioural responses of all 3842 workers. We find that strict specialization is disadvantageous for a colony's annual reproduction and growth during slave raids. These fitness costs may favour generalist strategies in dynamic environments, as we also demonstrate that societies exposed to slavemakers in the field show a lower degree of specialization than those originating from slavemaker-free populations. Our findings provide an explanation for the ubiquity of generalists and highlight their importance for the flexibility and functional robustness of entire societies.