Date Published: October 24, 2018
Publisher: Public Library of Science
Author(s): Laura Beani, Federico Cappa, Fabio Manfredini, Marco Zaccaroni, Renee M. Borges.
The parasitic insect Xenos vesparum induces noticeable behavioral and physiological changes—e.g. castration—in its female host, the paper wasp Polistes dominula: parasitized putative workers avoid any colony task and desert the colony to survive in the nearby vegetation, like future queens and males do. In this long-term observational study, we describe the spectacular attraction of parasitized workers towards trumpet creeper bushes (Campsis radicans) in early-summer. Two thirds of all wasps that we sampled on these bushes were parasitized, whereas the parasite prevalence was much lower in our study area and most wasps sampled on other nearby flowering bushes were non-parasitized. First, we describe the occurrence and consistency of this phenomenon across different sites and years. Second, we evaluate the spatial behavior of parasitized wasps on C. radicans bushes, which includes site-fidelity, exploitation and defense of rich extra-floral nectaries on buds and calices. Third, we record two critical steps of the lifecycle of X. vesparum on C. radicans: the parasite’s mating and a summer release of parasitic larvae, that can infect larval stages of the host if transported to the host’s nest. In a nutshell, C. radicans bushes provide many benefits both to the parasite X. vesparum and to its host: they facilitate the parasite’s mating and bivoltine lifecycle, a phenomenon never described before for this parasite, while, at the same time, they provide the wasp host with shelter inside trumpet flowers and extrafloral gland secretions, thus likely enhancing host survival and making it a suitable vector for the infection.
Social insects are prime targets of parasites that can find suitable conditions within insect colonies to spread . The primitively eusocial wasp Polistes dominula (Hymenoptera, Vespidae) is the host of the endoparasitic insect Xenos vesparum (Strepsiptera, Xenidae). This parasite is capable to induce significant modifications in the host physiology (including castration, [2–4]) and behavior. If parasitized by X. vesparum, P. dominula workers do not participate in colony tasks (e.g., they do not contribute to rearing siblings), do not receive aggressions by nest-mates and behave instead like future queens, i.e. they desert the nest to form summer aggregations on selected vegetation nearby [5–7]. This is a striking unusual behavior in a model organism for social evolution , and a recent study has shown a significant shift in the expression of caste-related genes that is associated with parasitism . These off-season “estivation/hibernation gatherings”, first described by Hamilton , have been extensively documented in the past because they are aberrant and conspicuous, located for days on the same leaves, with a 98% parasite prevalence . They usually occur in August and September in Tuscany (i.e. late in the wasp colony cycle) and include putative workers that have deserted the colony in June and July (hereafter defined as “parasitized workers”), and castrated putative queens that emerged and departed from their colony in August .
The current imbalance between empirical and theoretical studies on host manipulation by parasites  prompted us to describe the spatial and feeding behavior of P. dominula workers parasitized by X. vesparum in the field. These wasps are less conspicuous than wasps that form late-summer or winter aggregations. Nevertheless, we were able to describe their behavior in details thanks to the fortunate discovery of their consistent occurrence on C. radicans bushes over time and in different locations. Our observations show that parasitized P. dominula workers have a clear preference for C. radicans. Year after year, two-thirds of workers collected on these plants were parasitized, in comparison to only 6% as observed on other flowering bushes, which were intensively patrolled by non-parasitized wasps instead. This is an unexpectedly high rate, considering that the parasite prevalence in our study area is lower than in trumpet creepers (proportion of infected larvae and pupae per nest = 0.16 ± 0.7 ; proportion of infected adults in winter aggregations: between 0.10 and 0.25). A recent screening on 14 parasitized nests, collected in Sesto area, confirms that 13.39% of workers were parasitized (30 out of 124 wasps emerged from these lab nests between June and July 2017, pers. obs.).