RESUMO
Seemingly small ecological changes can have large, ramifying effects that defy expectations. Such are keystone effects in ecosystems. Phloem-feeding insect herbivores can act as keystone species by altering community structure and species interactions via plant-mediated or ant-mediated mechanisms. Plant responses triggered by phloem feeders can disrupt tri-trophic interactions induced by leaf-chewing herbivores, while ants that tend phloem feeders can deter or prey on other arthropods. Here, we investigate how phloem-feeding herbivores change caterpillar-parasitoid interactions on Quercus alba (white oak) trees in natural forests. We factorially manipulated the presence of phloem-feeding insects as well as ant access on Q. alba branches over multiple years and sites and measured parasitism rates of co-occurring caterpillars. While 19.3% of caterpillars were parasitized when phloem feeders were removed, the presence of phloem feeders completely suppressed parasitism of caterpillars (0%). This stark pattern was consistent across the diverse community of phloem feeders and caterpillars. Our manipulation of ant access had no effect on parasitism of caterpillars, implicating a plant-mediated mechanism. We further assessed the mechanistic hypothesis that phloem feeders suppress plant emission of caterpillar-induced volatile compounds, which could disrupt host-location behavior by parasitoids of caterpillars. Phloem feeders indeed reduced concentrations of four volatile compounds, consistent with the putative plant volatile-mediated mechanism. Given the important role of parasitoids in controlling herbivore populations, this keystone effect of phloem feeders offers novel insight into community dynamics in forests and potentially other terrestrial ecosystems.
Assuntos
Formigas , Herbivoria , Larva , Floema , Quercus , Animais , Larva/fisiologia , Larva/parasitologia , Quercus/parasitologia , Quercus/fisiologia , Floema/parasitologia , Formigas/parasitologia , Formigas/fisiologia , Interações Hospedeiro-Parasita , Mariposas/parasitologia , Mariposas/fisiologia , Florestas , Cadeia AlimentarRESUMO
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.
Assuntos
Formigas , Fenótipo , Formigas/fisiologia , Formigas/microbiologia , Formigas/parasitologia , Animais , Hypocreales/fisiologia , Brasil , Comportamento Animal/fisiologia , Interações Hospedeiro-Parasita/fisiologiaRESUMO
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.
Assuntos
Formigas , Estudo de Associação Genômica Ampla , Polimorfismo de Nucleotídeo Único , Receptores Odorantes , Animais , Formigas/genética , Formigas/parasitologia , Receptores Odorantes/genética , Clima , Interações Hospedeiro-Parasita/genética , Adaptação Fisiológica/genética , Odorantes , Hidrocarbonetos/metabolismoRESUMO
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.
Assuntos
Formigas , Parasitos , Animais , Formigas/parasitologia , Evolução Biológica , Interações Hospedeiro-Parasita , Filogenia , Comportamento Social , SimbioseRESUMO
Ant nest beetles (Carabidae, Paussinae, Paussini; Paussus) are renowned myrmecophiles, mostly known for their bizarre and diverse antennal shape. While little is known about their development, behavior and host range, we do know they spend most of their lives inside ant nests, feeding upon the hemolymph of ant brood and teneral workers. Recent findings suggest these beetles use a surprisingly complex strategy for interacting and deceiving ants. They have managed to break into multiple communication channels that ants use to recognize and communicate with one another in order to deceive the ants and profit from the rich resources of the nest. Mounting evidence from structural, chemical, acoustic, and behavioral studies support the hypothesis that Paussus is among the most highly integrated parasite of social insects known to date.
Assuntos
Formigas , Besouros , Acústica , Animais , Formigas/parasitologiaRESUMO
The rise of ants over the past ~100 million years reshaped the biosphere, presenting ecological challenges for many organisms, but also opportunities. No insect group has been so adept at exploiting niches inside ant colonies as the rove beetles (Staphylinidae) - a global clade of>64,000 predominantly free-living predators from which numerous socially parasitic 'myrmecophile' lineages have emerged. Myrmecophilous staphylinids are specialized for colony life through changes in behavior, chemistry, anatomy, and life history that are often strikingly convergent, and hence potentially adaptive for this symbiotic way of life. Here, we examine how the interplay between ecological pressures and molecular, cellular, and neurobiological mechanisms shape the evolutionary trajectories of symbiotic lineages in this ancient, convergent system.
Assuntos
Formigas , Besouros , Animais , Formigas/parasitologia , Evolução Biológica , Besouros/anatomia & histologia , SimbioseRESUMO
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.
Assuntos
Formigas , Hypocreales , Animais , Formigas/genética , Formigas/microbiologia , Formigas/parasitologia , Comportamento Animal , Hypocreales/genética , TranscriptomaRESUMO
Polyrhachis lamellidens is a temporary social parasitic species. When a newly mated queen encounters a host worker, it opens its jaws and then mounts and rubs the body of the host worker, called rubbing behaviour. This behaviour is different from aggressive behaviour and is considered to be a preparatory action before invasion of the host colony. However, it is unclear what cues trigger rubbing behaviour. Therefore, in this study, we used glass beads that imitated the insect body surfaces and searched for triggers. Although P. lamellidens did not respond to the cuticular compounds only, cuticular compounds and chitin coatings on glass beads elicited responses that were similar to those towards live samples. The rubbing behaviour of P. lamellidens was elicited in response to a cuticle-like surface that mimicked a procuticle by combining the compounds with chitin. These results suggest that host recognition and nest-mate recognition are supported by different mechanisms. This article has an associated First Person interview with the first author of the paper.
Assuntos
Formigas , Animais , Formigas/parasitologia , Formigas/fisiologia , HumanosRESUMO
Social parasitism describes a fascinating way of life in which species exploit the altruistic behaviour of closely related, social species. Social parasites have repeatedly evolved in the social Hymenoptera, including ants, bees, and wasps. The common ancestry and shared (social) environment with their hosts facilitates the study of molecular adaptations to the parasitic lifestyle. Moreover, when social parasites are widespread and virulent, they exert strong selection pressure on their hosts, leading to the evolution of defense mechanisms and triggering a coevolutionary arms race. Recent advances in sequencing technology now make it possible to study the molecular basis of this coevolutionary process. In addition to describing the latest developments, we highlight open research questions that could be tackled with genomic, transcriptomic, or epigenetic data.
Assuntos
Formigas , Parasitos , Vespas , Animais , Formigas/genética , Formigas/parasitologia , Abelhas , Interações Hospedeiro-Parasita/genética , Simbiose , Vespas/genéticaRESUMO
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.
Assuntos
Formigas/microbiologia , Formigas/parasitologia , Borboletas , Fungos , Interações entre Hospedeiro e Microrganismos , Interações Hospedeiro-Parasita , Animais , Meio AmbienteRESUMO
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.
Assuntos
Formigas , Dípteros , Interações Hospedeiro-Parasita , Animais , Formigas/parasitologia , Dípteros/patogenicidade , Interações Hospedeiro-Parasita/fisiologia , Simbiose/fisiologiaRESUMO
Most species are either parasites or exploited by parasites, making parasite-host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes' transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.
Assuntos
Formigas , Cestoides/fisiologia , Regulação da Expressão Gênica/imunologia , Interações Hospedeiro-Parasita , Proteínas de Insetos , Animais , Formigas/genética , Formigas/imunologia , Formigas/parasitologia , Interações Hospedeiro-Parasita/genética , Interações Hospedeiro-Parasita/imunologia , Proteínas de Insetos/genética , Proteínas de Insetos/imunologiaRESUMO
The social parasitic beetle Paussus favieri (Coleoptera, Carabidae, Paussini) performs different types of stridulations, which selectively mimic those emitted by different ant castes of its host Pheidole pallidula (Hymenoptera, Formicidae, Myrmicinae). However, the significance of this acoustical mimicry for the success of the parasitic strategy and the behaviors elicited in the host ants by stridulations was unknown. We reared Paussus favieri in Pheidole pallidula colonies and filmed their interacting behaviors. We analyzed in slow motion the behavior of ants near a stridulating beetle. We analyzed separately trains of pulse (Pa + Pb, produced by repeated rubbings) and single pulse (Pc, produced by a single rubbing) of stridulations, clearly recognizable from the shaking up and down of the beetle hind legs, and associated them with different ant responses. The full repertoire of sounds produced by P. favieri elicited benevolent responses both in workers and soldiers. We found that different signals elicit different (sometimes multiple) behaviors in ants, with different frequency in the two ant castes. However, Pc (alone or in conjunction with other types of pulses) appears to be the type of acoustic signal mostly responsible for all recorded behaviors. These results indicate that the acoustic channel plays a pivotal role in the host-parasite interaction. Finding that a parasite uses the acoustical channel so intensively, and in such a complicated way to trigger ant behaviors, indicates that acoustic signals may be more important in ant societies than commonly recognized.
Assuntos
Comunicação Animal , Formigas/parasitologia , Percepção Auditiva , Besouros/fisiologia , Interações Hospedeiro-Parasita/fisiologia , Acústica , AnimaisRESUMO
Clavigeritae is a group of obligate myrmecophiles of the rove beetle subfamily Pselaphinae (Staphylinidae). Some are blind and wingless, and all are believed to depend on ant hosts through feeding by trophallaxis. Phylogenetic hypotheses suggest that their ancestors, as are most pselaphines today, were free-living predators. Morphological alterations required to transform such beetles into extreme myrmecophiles were poorly understood. By studying the cephalic morphology of Claviger testaceus, we demonstrate that profound changes in all mouthpart components took place during this process, with a highly unusual connection of the maxillae to the hypopharynx, and formation of a uniquely transformed labium with a vestigial prementum. The primary sensory function of the modified maxillary and labial palps is reduced, and the ventral mouthparts transformed into a licking/'sponging' device. Many muscles have been reduced, in relation to the coleopteran groundplan or other staphylinoids. The head capsule contains voluminous glands whose appeasement secretions are crucial for the beetle survival in ant colonies. The brain, in turn, has been shifted into the neck region. The prepharyngeal dilator is composed of an entire series of bundles. However, the pharynx does not show any peculiar adaptations to taking up liquid food. We demonstrate that far-reaching cephalic modifications characterize C. testaceus, and that the development of appeasement glands and adaptation of the mouthparts to trophallaxis determine the head architecture of this extreme myrmecophile.
Assuntos
Adaptação Fisiológica , Formigas/parasitologia , Besouros/anatomia & histologia , Cabeça/anatomia & histologia , Animais , Antenas de Artrópodes/anatomia & histologia , Osso e Ossos/anatomia & histologia , Besouros/ultraestrutura , Mandíbula/anatomia & histologia , Músculos/anatomia & histologia , Sistema Nervoso/anatomia & histologia , Sistema Nervoso/diagnóstico por imagem , Faringe/anatomia & histologia , Filogenia , Microtomografia por Raio-XRESUMO
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.
Assuntos
Formigas/parasitologia , Doenças do Cão/diagnóstico , Doenças do Cão/patologia , Leishmaniose Visceral/patologia , Animais , Teorema de Bayes , Brasil/epidemiologia , Doenças do Cão/epidemiologia , Cães , Humanos , Leishmania infantum/isolamento & purificação , Leishmaniose Visceral/epidemiologia , Distribuição de Poisson , Fatores de Risco , Estudos SoroepidemiológicosRESUMO
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.
Assuntos
Evolução Biológica , Interações Hospedeiro-Parasita/fisiologia , Parasitos/fisiologia , Animais , Formigas/parasitologia , Formigas/fisiologia , Comportamento Animal , Dicrocoelium/parasitologia , Interações Hospedeiro-Parasita/genética , Larva , Linhagem , Caramujos/parasitologia , Trematódeos/genética , Trematódeos/fisiologiaRESUMO
Ants have been shown to engage in symbiosis across the tree of life, although our knowledge is far from complete. These interactions range from mutualistic to parasitic with several instances of manipulation of host behavior. Nutrient contributions in these symbioses include both farming for food and nitrogen recycling by gut-associated microbes. Interestingly, the ants that are mostly likely to host diverse and likely functional gut microbial communities are those that feed on extreme diets. Although we do see many instances of symbiosis between ants and microbes, there are also examples of species without a functional gut microbiome. Symbiosis among microbes and eukaryotic hosts is common and often considered a hallmark of multicellular evolution [1]. This is true among many of the over 13000 species of ants, although symbiosis between ants and microbes are not ubiquitous. These microbial-ant symbiotic interactions span the tree of life and include microbial eukaryotes, fungi, viruses, and bacteria. These interactions range from pathogenic to mutualistic, with many relationships still not well understood. Although our knowledge of the diversity of these microbes in ants is growing rapidly, and in some cases we know the function and interaction with the host, we still have much to learn about - the little things that run the little things that run the world!
Assuntos
Formigas , Simbiose , Animais , Formigas/microbiologia , Formigas/parasitologia , Bactérias , Comportamento , Dieta , Fungos , Microbioma Gastrointestinal , Interações Hospedeiro-Parasita , Microbiota , Nematoides , Trematódeos , VírusRESUMO
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.
Assuntos
Formigas/metabolismo , Formigas/parasitologia , Dípteros/classificação , Adaptação Fisiológica , Animais , Evolução Biológica , Comportamento Alimentar , Cromatografia Gasosa-Espectrometria de Massas/métodos , Genética Populacional/classificação , Especificidade de Hospedeiro , Interações Hospedeiro-Parasita , Hidrocarbonetos/química , Larva/metabolismo , Comportamento SocialRESUMO
The manipulation of animal behavior by parasitic organisms is one of the most complex adaptations to have arisen via natural selection. Among the most impressive examples of behavioral manipulation are the zombie-ant fungi [1]. In this association, ants are controlled to leave the colony and perform a stereotyped death grip behavior, where they bite onto vegetation over foraging trails, before being killed for the post mortem fungal growth. Manipulation functions to provide a platform outside the nest, from which fungal parasites actively shoot out spores, targeting foraging ants because within colony transmission is prevented by strong social immunity exhibited by social insect societies [2, 3]. It is not clear how such complex examples of host manipulation arose. To address this, we performed a broad-scale phylogenetic reconstruction of the order Hypocreales, to which the zombie-ant fungi, Ophiocordyceps, belong. In order to understand the patterns of host association and host switching along the evolution of Ophiocordyceps, we performed ancestral character state reconstruction analysis. We found that zombie-ant fungi likely arose from an ancestor that infected beetle larvae residing in soil or decaying wood, similar to extant beetle-infecting Ophiocordyceps species. Surprisingly, the jump led to an extensive species radiation observed after the development of behavioral manipulation. We suggest that the jump from solitary beetle larva to ants within a colony exposed the fungus to the robust social immunity of ant societies.