Transcriptomics of an extended phenotype: parasite manipulation of wasp social behaviour shifts expression of caste-related genes

Abstract

Parasites can manipulate host behaviour to increase their own transmission and fitness, but the genomic mechanisms by which parasites manipulate hosts are not well understood. We investigated the relationship between the social paper wasp, Polistes dominula, and its parasite, Xenos vesparum (Insecta: Strepsiptera), to understand the effects of an obligate endoparasitoid on its host's brain transcriptome. Previous research suggests that X. vesparum shifts aspects of host social caste-related behaviour and physiology in ways that benefit the parasitoid. We hypothesized that X. vesparum-infested (stylopized) females would show a shift in caste-related brain gene expression. Specifically, we predicted that stylopized females, who would normally be workers, would show gene expression patterns resembling pre-overwintering queens (gynes), reflecting gyne-like changes in behaviour. We used RNA-sequencing data to characterize patterns of brain gene expression in stylopized females and compared these with those of unstylopized workers and gynes. In support of our hypothesis, we found that stylopized females, despite sharing numerous physiological and life-history characteristics with members of the worker caste, show gyne-shifted brain expression patterns. These data suggest that the parasitoid affects its host by exploiting phenotypic plasticity related to social caste, thus shifting naturally occurring social behaviour in a way that is beneficial to the parasitoid.

Keywords: eusociality; gene expression; host–parasite interactions; parasite manipulation; social caste; social wasp.

Figure 1.

Polistes dominula host and Xenos vesparum parasite life cycle. Stylopized wasps indicated with red outline. Letters indicate P. dominula life cycle: (A) founding phase, (B) worker phase, (C) reproductive phase, (D) decline and (E) overwintering aggregation. Numbers indicate X. vesparum life cycle: (1) first-instar X. vesparum larvae infect host P. dominula larvae in the nest, (2) endoparasitic larvae develop inside host pupa, (3) male cephalotheca/female cephalothorax extrudes from between-host tergites, (4) aberrant aggregations: male X. vesparum emerge as free-living adults and mate, then die; neotenic females remain endoparasitic in hosts, (5) stylopized wasps joined by unstylopized gynes to overwinter, (6) stylopized wasps leave aggregation after unstylopized gynes have begun founding, (7) stylopized wasps forage and visit conspecific nests, but do not found nests themselves. Female X. vesparum drops first-instar larvae directly on nests or on flowers (drawing not to scale, by A.C. Geffre) (Online version in colour.)

Figure 2.

(a) Heatmap showing summary of mean expression patterns for each group (worker (W), stylopized (S) and gyne (G)), and clustered both by transcript (rows) and groups (columns). Red represents downregulation and green represents upregulation (relative to the mean for each gene). The results show that overall gene expression patterns for S and G are most similar. (b) Venn diagram of the number of DETs in pairwise comparisons between groups (created in Venny [50]), highlighting the most promising ‘parasite manipulation candidate genes’. (c) Pearson correlation of logged fraction of worker read counts (RC) among gynes and stylopized females across the 16 shared DETs (from worker versus gyne and stylopized versus worker comparisons), R² = 0.9831, p < 0.001. (Online version in colour.)

Figure 3.

Validation of RNA-seq results using qRT-PCR. Normalized expression is considered as a percentage increase or decrease of expression compared with that of the worker group (i.e. W = 1 = 100% worker expression). Sample sizes shown below the bars, statistical significance indicated with *. (a) Defensin expression was similar in both qRT-PCR and RNA-seq experiments. Expression levels significantly different with RNA-seq (indicated by *), but not qRT-PCR. (b) IRP30 expression was also similar in both RNA-seq and qRT-PCR. Expression levels were significantly different with RNA-seq (indicated by *) and also qRT-PCR when normalized by actin (Wilcoxon: χ² = 6.1091, p = 0.0471) or normalized by Ef-1 (Wilcoxon: χ² = 6.303, p = 0.0428).