Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?

Abstract

Paper wasps (Polistes dominula), parasitized by the strepsipteran Xenos vesparum, are castrated and desert the colony to gather on plants where the parasite mates and releases primary larvae, thus completing its lifecycle. One of these plants is the trumpet creeper Campsis radicans: in a previous study the majority of all wasps collected from this plant were parasitized and focused their foraging activity on C. radicans buds. The unexpected prevalence and unusual feeding strategy prompted us to investigate the influence of this plant on wasp behavior and physiology through a multidisciplinary approach. First, in a series of laboratory bioassays, we observed that parasitized wasps spent more time than non-parasitized ones on fresh C. radicans buds, rich of extra-floral nectaries (EFNs), while the same wasps ignored treated buds that lacked nectar drops. Then, we described the structure and ultra-structure of EFNs secreting cells, compatible with the synthesis of phenolic compounds. Subsequently, we analysed extracts from different bud tissues by HPLC-DAD-MS and found that verbascoside was the most abundant bioactive molecule in those tissues rich in EFNs. Finally, we tested the immune-stimulant properties of verbascoside, as the biochemical nature of this compound indicates it might function as an antibacterial and antioxidant. We measured bacterial clearance in wasps, as a proxy for overall immune competence, and observed that it was enhanced after administration of verbascoside—even more so if the wasp was parasitized. We hypothesize that the parasite manipulates wasp behavior to preferentially feed on C. radicans EFNs, since the bioactive properties of verbascoside likely increase host survival and thus the parasite own fitness.

A Strepsipteran parasite extends the lifespan of workers in a social wasp

“…In contrast, we found the opposite result, as the majority of the workers parasitized by large female parasites survived at least 6 months longer than those parasitized by males. In captivity, similarly to what observed in the field 28 , 29 , twisted-winged X. vesparum males emerged from their puparium, successfully fertilized females (71%) and died a few hours later. Workers harboring a male died in the summer, shortly after the emergence of the parasite (Fig.…”

“…Despite the possible survival costs associated with the activation of the immune system in response to a parasite 46 , 65% of workers infected by a Xenos female survived until the experimental dissection at the end of March. The altered feeding frequency 28 , 29 of parasitized wasps on trumpet creepers, source of our experimental sample, might be a compensatory behavior that increases the uptake of nutrients and immune-stimulating substances 47 . Indeed, a key factor for winter survival is resource storage 48 – 50 , as fat bodies release energy during prolonged non-feeding periods as hibernation 51 .…”

“…The flexible caste determination mechanism of Polistes dominula 22 , 23 is exploited by the strepsipteran Xenos vesparum (Xenidae), a parasitic castrator that usurps the host reproductive resources to complete its life cycle 24 . Parasitized P. dominula females, the primary host 25 , 26 , do not develop ovaries, desert the colony early in the season without performing any social task 27 and forage on selected plants, rich of extra-floral nectaries secreting immune-stimulant compounds 28 , 29 . They form aberrant summer aggregations, where parasite mating occurs 30 , and may overwinter in sheltered sites with future queens 31 .…”

“…The female parasite is the reservoir of 1st instar larvae that can infect all larval stages of P. dominula 35 : these are the so-called triungulins, which are released on flowers or directly on nests by parasitized wasps 36 , 37 . The parasite cycle is bivoltine: there are two releases of triungulins, the first targeting worker wasps in the spring, the second targeting wasp sexuals in the summer 29 . Intriguingly, the effects of parasitic manipulation appear to depend on host sex; parasitized male wasps retain their sexual behaviour, die at the end of the summer and are absent from overwintering wasps’ aggregations 31 .…”

“…To date, the survival of parasitized workers until the following spring has been only hypothesized 26 , 31 , 33 , 34 . Thus, in the present work, a substantial sample of workers were collected from flowering trumpet creepers in July (at a time when colonies do not yet produce sexuals), when parasitized wasps began to feed and aggregate on these bushes 28 , 29 , and were caged until March to assess their lifespan. We measured survival rates and a set of morpho-physiological traits (wasp size, abdominal lipid stores, ovary development) known to influence caste differentiation in Polistes 38 .…”