Search

Hosts can carry many viruses in their bodies, but not all of them cause disease. We studied ants as a social host to determine both their overall viral repertoire and the subset of actively infecting viruses across natural populations of three subfamilies: the Argentine ant (Linepithema humile, Dolichoderinae), the invasive garden ant (Lasius neglectus, Formicinae) and the red ant (Myrmica rubra, Myrmicinae). We used a dual sequencing strategy to reconstruct complete virus genomes by RNA-seq and to simultaneously determine the small interfering RNAs (siRNAs) by small RNA sequencing (sRNA-seq), which constitute the host antiviral RNAi immune response. This approach led to the discovery of 41 novel viruses in ants and revealed a host-ant specific RNAi response (21 vs. 22 nt siRNAs) in the different ant species. The efficiency of the RNAi response (sRNA/RNA read count ratio) depended on the virus and the respective ant species, but not its population. Overall, we found the highest virus abundance and diversity per population inLi. humile, followed byLa. neglectusandM. rubra. Argentine ants also shared a high proportion of viruses between populations, whilst overlap was nearly absent inM. rubra. Only a single of the total 59 viruses in our study caused active infection in more than one ant species, whilst six viruses infected one, but only contaminated another ant species. Disentangling active infection from contamination thus allowed us to show high host-specificity of active viral infections versus a decent degree of spillover of non-infecting viral contaminants across ant species, providing relevant information for ecosystem management.

The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris ) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Social insect colonies have evolved many collectively performed adaptations that reduce the impact of infectious disease and that are expected to maximize their fitness. This colony-level protection is termed social immunity, and it enhances the health and survival of the colony. In this review, we address how social immunity emerges from its mechanistic components to produce colony-level disease avoidance, resistance, and tolerance. To understand the evolutionary causes and consequences of social immunity, we highlight the need for studies that evaluate the effects of social immunity on colony fitness. We discuss the roles that host life history and ecology have on predicted eco-evolutionary dynamics, which differ among the social insect lineages. Throughout the review, we highlight current gaps in our knowledge and promising avenues for future research, which we hope will bring us closer to an integrated understanding of socio-eco-evo-immunology.

Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly1 and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops2. Honey bees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high impact pathogens3,4 and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumble bees (Bombus spp.) are in global decline5,6, one cause of which may be pathogen spillover from managed pollinators like honey bees7,8 or commercial colonies of bumble bees9. In our study, a combination of infection experiments with landscape scale field data indicates that honey bee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic Nosema ceranae is linked between honey bees and bumble bees, with honey bees having higher DWV prevalence, and sympatric bumble bees and honey bees sharing DWV strains; Apis is therefore the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates10,11 highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.

Summary Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security. RNA viruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood. This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range of RNA viruses. Within a structured large-scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multiple RNA viruses in co-occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombus spp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators. Multiple RNA viruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species-specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least one RNA virus, prevalence is higher in wild bumblebees than in managed honeybee populations. Our findings indicate widespread transmission of RNA viruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline.

Parasitic Maculinea alcon butterflies can only develop in nests of a subset of available Myrmica ant species, so female butterflies have been hypothesized to preferentially lay eggs on plants close to colonies of the correct host ants. Previous correlational investigations of host-ant-dependent oviposition in this and other Maculinea species have, however, shown equivocal results, leading to a long-term controversy over support for this hypothesis. We therefore conducted a controlled field experiment to study the egg-laying behaviour of M. alcon . Matched potted Gentiana plants were set out close to host-ant nests and non-host-ant nests, and the number and position of eggs attached were assessed. Our results show no evidence for host-ant-based oviposition in M. alcon , but support an oviposition strategy based on plant characteristics. This suggests that careful management of host-ant distribution is necessary for conservation of this endangered butterfly.

Social insect colonies are like fortresses, well protected and rich in shared stored resources. This makes them ideal targets for exploitation by predators, parasites and competitors. Colonies of Myrmica rubra ants are sometimes exploited by the parasitic butterfly Maculinea alcon . Maculinea alcon gains access to the ants' nests by mimicking their cuticular hydrocarbon recognition cues, which allows the parasites to blend in with their host ants. Myrmica rubra may be particularly susceptible to exploitation in this fashion as it has large, polydomous colonies with many queens and a very viscous population structure. We studied the mutual aggressive behaviour of My. rubra colonies based on predictions for recognition effectiveness. Three hypotheses were tested: first, that aggression increases with distance (geographical, genetic and chemical); second, that the more queens present in a colony and therefore the less-related workers within a colony, the less aggressively they will behave; and that colonies facing parasitism will be more aggressive than colonies experiencing less parasite pressure. Our results confirm all these predictions, supporting flexible aggression behaviour in Myrmica ants depending on context.

Most animal societies are non-clonal and thus subject to conflicts. In social insects, conflict over male production can be resolved by worker policing, i.e. eating of worker-laid eggs (WLE) or aggression towards reproductive workers. All workers in a colony have an interest in policing behaviour being expressed, but there can be asymmetries among workers in performing the actual behaviour. Here, we show that workers of the ant Pachycondyla inversa specialize in policing behaviour. In two types of behavioural assays, workers developed their ovaries and laid eggs. In the first experiment, reproductive workers were introduced into queenright colonies. In the second experiment, WLE were introduced. By observing which individuals policed, we found that aggressive policing was highly skewed among workers that had opportunity to police, and that a similar tendency occurred in egg policing. None of the policing workers had active ovaries, so that policing did not incur a direct selfish benefit to the policer. This suggests that policing is subject to polyethism, just like other tasks in the colony. We discuss several hypotheses on the possible causes of this skew in policing tasks. This is the first non-primate example of specialization in policing tasks without direct selfish interests. ispartof: Proceedings of the Royal Society of London vol:274 issue:1616 pages:1421-1428 ispartof: location:England status: published