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Research article - Peer-reviewed, 2021

Comparative dissection of the peripheral olfactory system of the Chagas disease vectors Rhodnius prolixus and Rhodnius brethesi

Campetella, Florencia; Ignell, Rickard; Beutel, Rolf; Hansson, Bill S.; Sachse, Silke


American trypanosomiasis, or Chagas disease, is transmitted by both domestic and sylvatic species of Triatominae which use sensory cues to locate their vertebrate hosts. Among them, odorants have been shown to play a key role. Previous work revealed morphological differences in the sensory apparatus of different species of Triatomines, but to date a comparative functional study of the olfactory system is lacking. After examining the antennal sensilla with scanning electronic microscopy (SEM), we compared olfactory responses of Rhodnius prolixus and the sylvatic Rhodnius brethesi using an electrophysiological approach. In electroantennogram (EAG) recordings, we first showed that the antenna of R. prolixus is highly responsive to carboxylic acids, compounds found in their habitat and the headspace of their vertebrate hosts. We then compared responses from olfactory sensory neurons (OSNs) housed in the grooved peg sensilla of both species, as these are tuned to these compounds using single-sensillum recordings (SSRs). In R. prolixus, the SSR responses revealed a narrower tuning breath than its sylvatic sibling, with the latter showing responses to a broader range of chemical classes. Additionally, we observed significant differences between these two species in their response to particular volatiles, such as amyl acetate and butyryl chloride. In summary, the closely related, but ecologically differentiated R. prolixus and R. brethesi display distinct differences in their olfactory functions. Considering the ongoing rapid destruction of the natural habitat of sylvatic species and the likely shift towards environments shaped by humans, we expect that our results will contribute to the design of efficient vector control strategies in the future.Author summaryAn estimated eight million people worldwide are infected with American trypanosomiasis, also known as Chagas disease, whose causative agent is the parasite Trypanosoma cruzi. Over a hundred species of insects belonging to the Tritatomine subfamily are vectors of the disease, as they spread T. cruzi through their feaces. Several studies have highlighted the importance of olfaction for host-seeking behavior in these insects, which enables them to locate their vertebrate hosts and to obtain their vital blood meal. Vector control strategies have been the most efficient policy to combat the spread of Chagas disease by triatomine insects. However, recent changes in the natural habitats of these insects challenge the efficacy of these strategies, as species so far thought to be exclusive to sylvatic environments are now frequently found in peridomestic areas. In this context, understanding how triatomines with different distributions detect odors to locate their hosts and choose their habitats is highly relevant. In this study, we compare the olfactory system of the widely distributed Rhodnius prolixus and a sylvatic sibling Rhodnius brethesi at a morphological and functional level. We reveal that detection of host and habitat volatiles share many similarities, but also exhibit pronounced differences between species.

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2021, Volume: 15, number: 4, article number: e0009098

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