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

Abstract

American trypanosomiasis or Chagas disease is thought to be transmitted by both domestic and sylvatic species of Triatominae. These haematophagous insects use sensory cues to find their vertebrate hosts. Among them, odorants have been shown to play a key role. Previous work revealed morphological differences in the sensory apparatus of sylvatic and domestic species of Triatomines, but to date a functional study of the olfactory system is not available. After examining the antennal sensilla with scanning electronic microscopy (SEM), we compared olfactory responses of the domestic Rhodnius prolixus and the sylvatic Rhodnius brethesi with an electrophysiological approach. In electroantennogram (EAG) recordings, we first show that the antenna of R. prolixus shows high responses to carboxylic acids, compounds found in their habitat and headspace of 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 (SSR). In R. prolixus, the SSR responses revealed a narrower tuning breath than its sylvatic counterpart, 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 likely shifts towards environments shaped by humans, we expect that our results will contribute to the design of efficient vector control strategies in the future. Author SummaryAmerican Tripanosomiasis, also known as Chagas disease, is a disease which no one speaks out, although there are up to eight million people infected worldwide. Its causative agent is the protozoan Tripanosoma cruzi which is transmitted by triatomine insects, alias kissing bugs. Several studies have highlighted the importance of olfaction for host-seeking behavior in these insects, which enables them to target their vertebrate hosts, and to get their vital blood meal, while infecting them at the same time. 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 their effectiveness, as species so far thought to be exclusive to sylvatic environments are now frequently found in peridomestic areas. In this context, to understand how sylvatic and domestic kissing bugs detect odors to locate their host and choose their habitats is highly relevant. In this study, we compare the olfactory system of the domestic kissing bug Rhodnius prolixus and its sylvatic counterpart 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 both species.