Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output

Abstract

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.

Pathogen shifts in a honeybee predator following the arrival of the Varroa mite

“…This method of detection carries the risk of detecting false-positives. However, two lines of evidence support our finding of an active infection in wasps: (1) not all samples were positive in the strand-specific RT-PCR assay despite being positive for virus by standard PCR, indicating that the viral replication assay was able to differentiate between inactive and active virus; (2) previously published papers have demonstrated that honeybee viruses, including DWV, replicate in a variety of insects, including Vespula wasps [8,44,54]; thus, our finding of replication is not surprising.…”

Polyandry and paternity affect disease resistance in eusocial wasps: support for the parasite–pathogen hypothesis

“…responses among patrilines within colonies of the polyandrous V. vulgaris but they found no differences due to patriline, perhaps due to lower sample sizes than those employed here. Our results suggest that the PPH likely explains why high colony genetic diversity is associated with high reproductive success in eusocial wasps, as found by Goodisman et al (2007) and Dobelmann et al (2017). As observed in other Vespula species (Ross 1986;Goodisman et al 2007) we found that sperm mixing must have occurred in queens' spermatheca because patrilines were evenly distributed across emergence dates resulting in increased genetic diversity within colonies.…”

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp

“…Sex ratios in some social wasps can show considerable variation, with some colonies rearing predominantly either queens or males in their reproductive phase (Bonckaert, van Zweden, d'Ettorre, Billen, & Wenseleers ; Greene, ). Intracolony genetic diversity in Vespula wasps caused by multiple mating of the queen has been associated with variable sex ratios and queen production (Dobelmann et al, ; Goodisman et al, ; Johnson et al, ), indicating the importance of genetic diversity within a colony. However, observations for Vespula vulgaris suggest equal production of males and queens (Archer, , ), but it is not currently known whether these ratios can shift with invasion (Gloag et al, ).…”

“…Wasp colonies are annual and only produce one generation of males and new queens in late summer and autumn, and thus, the number of queen cells is a direct representation of the output of daughter queens for a queen or matriline. This estimate is commonly used to describe fitness in Vespula species (Archer, 1980;Dobelmann et al, 2017;Goodisman, Kovacs, & Hoffman, 2007) The Vespula germanica mitochondrial genome (GenBank Accession no. KR703583) was used as a reference, map generated using GenomeVx (Conant & Wolfe, 2008) [Colour figure can be viewed at wileyonlinelibrary.com] rearing predominantly either queens or males in their reproductive phase (Bonckaert, van Zweden, d'Ettorre, Billen, & Wenseleers 2011;Greene, 1984).…”

“…KR703583) was used as a reference, map generated using GenomeVx (Conant & Wolfe, 2008) [Colour figure can be viewed at wileyonlinelibrary.com] rearing predominantly either queens or males in their reproductive phase (Bonckaert, van Zweden, d'Ettorre, Billen, & Wenseleers 2011;Greene, 1984). Intracolony genetic diversity in Vespula wasps caused by multiple mating of the queen has been associated with variable sex ratios and queen production (Dobelmann et al, 2017;Goodisman et al, 2007;Johnson et al, 2009), indicating the importance of genetic diversity within a colony. However, observations…”