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Morphology of Stylops advarians (Strepsiptera) and the Effects of Parasitization on its Host, Andrena milwaukeensis (Hymenoptera)



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Strepsiptera is an enigmatic order of endoparasitic insects known for the extreme sexual dimorphism of the adults, which results in a unique lifecycle. Adult males are free-living, whereas adult females of most of the order’s taxa are neotenic and permanently endoparasitic. Stylops advarians Pierce, a parasite of Andrena milwaukeensis Graenicher, was collected in central Saskatchewan, Canada and verified to species according to the DNA sequencing analysis of a mitochondrial cytochrome oxidase I. The morphology of the adult male, and the structure of the adult female and first-instar larva, were examined. The adult male was described for the first time from the puparia of a single host. Notable features were the metathoracic scutellum, which reaches close to the prescutum, the antennae, with the fourth antennomere being less than twice as long as the fifth, and the hook-like aedeagus. Like other Stylops species, the adult female of S. advarians lacked many adult characteristics, with only her cephalothorax having identifiable features. Impact of the female parasite on her host was examined. Female bees that were stylopized by one or more parasitic females did not have any eggs, nor reproductive organs, within their abdomens, as opposed to non-stylopized bees. Internally within the host gaster, the foregut and partial midgut of bees with one female parasite were shifted away from the parasite. If two or three parasites were present, then the gaster’s components of the digestive tract were shifted below the parasites. The crop was heavily reduced in volume when parasitism occurred, but the hindgut was not greatly affected. The female parasites were found to reside above an air sac within their host’s gaster. First-instar larvae have several sensory structures on their head, including eye spots, olfactory pits, and numerous pairs of setae. On the legs, the pro- and mesothoracic tarsi are modified as adhesive structures, whereas those of the metathoracic legs are likely only used for movement. Similarly, the tips of the caudal filaments likely have an adhesive function, and the coarse hairs (spinulae) covering the thorax and abdomen on both dorsal and ventral surfaces likely help these larvae phoretically attach onto a host. For the first time, first-instars were reported on the surface of a non-stylopized host of A. milwaukeensis, as well as inside the crop of a non-stylopized A. milwaukeensis, likely as phoronts. Field-collection data for foraging bees of A. milwaukeensis was also recorded to determine seasonal occurrence of stylopization and different parameters of the parasite’s life history, including prevalence, intensity, and abundance, within this bee population. From greater than 450 bees taken over three consecutive years (2016–2018), from early May to late June, the prevalence of stylopized bees was found to be around 22% (21–24%). Despite attempts, males were not collected consistently, so their data are not included in this prevalence. The mean intensity of parasite infection was 1.2 (1.167–1.244) and parasite abundance was 0.27 (0.258–¬0.276), strongly suggesting that the current relationship of S. advarians parasitizing A. milwaukeensis, at this study site, is in balance. Stylopized female bees were found to emerge earlier than non-stylopized bees, possibly due to manipulation by the parasite. Mating of the parasites evidently occurred during this emergence, which was around May 2 each year. First-instar larvae began to emerge around May 22, suggesting mating takes place at similar times each year, and that the developmental period of the first-instars is short.



Strepsiptera, Stylops, parasitism, morphology, anatomy, host-parasite relationships, Hymenoptera, Andrena



Master of Science (M.Sc.)






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