Trypanosoma cruzi-infected Rhodnius prolixus endure increased predation facilitating parasite transmission to mammal hosts

PLoS Negl Trop Dis. 2021 Jul 1;15(7):e0009570. doi: 10.1371/journal.pntd.0009570. eCollection 2021 Jul.

Abstract

Triatomine bugs aggregate with conspecifics inside shelters during daylight hours. At dusk, they leave their refuges searching for hosts on which to blood feed. After finding a host, triatomines face the threat of being killed, because hosts often prey on them. As it is known that many parasites induce the predation of intermediate hosts to promote transmission, and that ingestion of Trypanosoma cruzi-infected bugs represents a very effective means for mammal infection, we hypothesized that trypanosomes induce infected bugs to take increased risk, and, as a consequence, be predated when approaching a host. Therefore, we evaluated whether the predation risk and predation rates endured by Rhodnius prolixus increase when infected with T. cruzi. Assays were performed in square glass arenas offering one central refuge to infected and uninfected 5th instar nymphs. A caged mouse was introduced in each arena after a three-day acclimation interval to activate sheltered insects and induce them to approach it. As hypothesized, a significantly higher proportion of infected insects was predated when compared with uninfected ones (36% and 19%, respectively). Indeed, T. cruzi-infected bugs took higher risk (Approximation Index = 0.642) when compared with healthy ones (Approximation Index = 0.302) and remained outside the shelters when the host was removed from the arena. Our results show that infection by T. cruzi induces bugs to assume higher risk and endure higher predation rates. We reveal a hitherto unknown trypanosome-vector interaction process that increases infected bug predation, promoting increased rates of robust oral transmission. The significant consequences of the mechanism revealed here make it a fundamental component for the resilient maintenance of sylvatic, peridomestic and domestic cycles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chickens
  • Host Specificity
  • Host-Parasite Interactions
  • Mice
  • Nymph / parasitology
  • Predatory Behavior
  • Rhodnius / parasitology*
  • Trypanosoma cruzi / physiology*

Grants and funding

AAG and MGL were supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq – Brazil productivity grants [AAG grant number 303546/2018-2; MGL grant number 311826/2019-9]. This work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais, FAPEMIG (AAG, grant numbers CRA-APQ-00569-15 and CRA-PPM-00162-17), Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, INCTEM/CNPq (AAG, MGL, grant number 465678/2014-9). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) (NPM, Finance Code 001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.