Emerging infectious diseases (EIDs) are a global threat to honeybees, and spillover from managed bees threaten wider insect populations. Deformed wing virus (DWV), a widespread virus that has become emergent in conjunction with the spread of the mite Varroa destructor, is thought to be partly responsible for global colony losses. The arrival of Varroa in honeybee populations causes a dramatic loss of viral genotypic diversity, favouring a few virulent strains. Here, we investigate DWV spillover in an invasive Hawaiian population of the wasp, Vespula pensylvanica, a honeybee predator and honey-raider. We show that Vespula underwent a parallel loss in DWV variant diversity upon the arrival of Varroa, despite the mite being a honeybee specialist. The observed shift in Vespula DWV and the variant-sharing between Vespula and Apis suggest that these wasps can acquire DWV directly or indirectly from honeybees. Apis prey items collected from Vespula foragers were positive for DWV, indicating predation is a possible route of transmission. We also sought cascading effects of DWV shifts in a broader Vespula pathogen community. We identified concurrent changes in a suite of additional pathogens, as well as shifts in the associations between these pathogens in Vespula. These findings reveal how hidden effects of the Varroa mite can, via spillover, transform the composition of pathogens in interacting species, with potential knock-on effects for entire pathogen communities.
Within any one habitat, the relative fitness of organisms in a population can vary substantially. Social insects like the common wasp are among the most successful invasive animals, but show enormous variation in nest size and other fitness‐related traits. Some of this variation may be caused by pathogens such as viruses that can have serious consequences in social insects, which range from reduced productivity to colony death. Both individual immune responses and colony‐level traits such as genetic diversity are likely to influence effects of pathogen infections on colony fitness. Here we investigate how infections with Kashmir Bee Virus (KBV), immune response and intracolony genetic diversity (due to queen polyandry) affect nest size in the invasive common wasp Vespula vulgaris. We show that KBV is highly prevalent in wasps and expression of antiviral immune genes is significantly increased with higher viral loads across individuals. Patriline membership within a nest did not influence KBV susceptibility or immune response. A permutational MANCOVA revealed that polyandry, viral load and expression of the immune gene Dicer were significant predictors of variation in nest size. High intracolony genetic diversity due to polyandry has previously been hypothesized to improve colony‐level resistance to parasites and pathogens. Consistent with this hypothesis, we observed genetically diverse colonies to be significantly larger and to produce more queens, although this effect was not driven by the pathogen we investigated. Invasive wasps clearly suffer from pathogens and expend resources, as indicated here by elevated immune gene expression, toward reducing pathogen‐impact on colony fitness.
Social insect colonies are pinnacles of evolved altruism but also exhibit dramatic conflict among relatives. In many species, a colony's workers compete with the queen and each other over the production of males. Interspecific comparisons demonstrate the importance of within-colony relatedness in determining the outcome of such conflicts, but facultative responses to within-colony relatedness are rarely reported. Here, I report facultative matricide (worker killing of a colony's queen) in the social wasp Dolichovespula arenaria. Matricide is strongly associated with high worker-worker relatedness, as predicted by theory, because closely related workers value nephews more than brothers. This pattern is the result of variation in both paternity frequency and the paternity skew of colonies with multiple patrilines, implicating worker-worker relatedness rather than a direct effect of multiple mating on queen survival. Furthermore, occasional inbreeding can explain why some multiple-patriline colonies exhibit high paternity skew associated with matricide. In general, these results support the hypothesis that workers can facultatively respond to intracolony relatedness determined by queen mating behavior and demonstrate a novel benefit of polyandry in annual social insects. Facultative matricide shows dramatically how workers are evolutionary actors with interests that can diverge from the queen's, rather than being "extrasomatic projections of her personal genome".
BackgroundThe puzzle of the selective benefits of multiple mating and multiple paternity in social insects has been a major focus of research in evolutionary biology. We examine paternity in a clade of social insects, the vespine wasps (the yellowjackets and hornets), which contains species with high multiple paternity as well as species with single paternity. This group is particularly useful for comparative analyses given the wide interspecific variation in paternity traits despite similar sociobiology and ecology of the species in the genera Vespula, Dolichovespula and Vespa. We describe the paternity of 5 species of yellowjackets (Vespula spp.) and we perform a phylogenetically controlled comparative analysis of relatedness, paternity frequency, paternity skew, colony size, and nest site across 22 vespine taxa.ResultsWe found moderate multiple paternity in four small-colony Vespula rufa-group species (effective paternity 1.5 – 2.1), and higher multiple paternity in the large-colony Vespula flavopilosa (effective paternity ~3.1). Our comparative analysis shows that colony size, but not nest site, predicts average intracolony relatedness. Underlying this pattern, we found that greater colony size is associated with both higher paternity frequency and reduced paternity skew.ConclusionsOur results support hypotheses focusing on the enhancement of genetic diversity in species with large colonies, and run counter to the hypothesis that multiple paternity is adaptively maintained due to sperm limitation associated with large colonies. We confirm the patterns observed in taxonomically widespread analyses by comparing closely related species of wasps with similar ecology, behavior and social organization. The vespine wasps may be a useful group for experimental investigation of the benefits of multiple paternity in the future.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0277-x) contains supplementary material, which is available to authorized users.
Social insect colonies exhibit a variety of life history strategies, from the annual, semelparous colonies of temperate bees and wasps to the long-lived colonies of many ants and honeybees. Species introduced to novel habitats may exhibit plasticity in life history strategies as a result of the introduction, but the factors governing these changes often remain obscure. Vespula pensylvanica, a yellowjacket wasp, exhibits such plasticity in colony longevity. Multi-year (perennial) colonies are relatively common in introduced populations in Hawaii, while source populations in the western United States are typically on an annual cycle. Here, we use experiments and observational data to examine how diet, disease, nest thermal environment, and nest location influence colony longevity in a population with both annual and perennial colonies. Counter to our predictions, experimental feeding and warming did not increase colony survival in the winter in the introduced range. However, Moku Virus load and wasp colony density predicted colony survival in one year, suggesting a potential role for disease in modulating colony phenology. We also found that local V. pensylvanica colony density was positively correlated with Moku Virus loads, and that Arsenophonus sp. bacterial loads in V. pensylvanica colonies were positively associated with proximity to feral honeybee (Apis mellifera) hives, suggesting potential transmission routes for these poorly understood symbionts. The factors influencing colony longevity in this population are likely multiple and interactive. More important than food availability, we propose winter precipitation as a critical factor that may explain temporal and spatial variation in colony longevity in these invasive wasps.
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