The interplay between temperature, Trypanosoma cruzi parasite load, and nutrition: Their effects on the development and life-cycle of the Chagas disease vector Rhodnius prolixus

PLoS Negl Trop Dis. 2024 Feb 2;18(2):e0011937. doi: 10.1371/journal.pntd.0011937. eCollection 2024 Feb.

Abstract

Chagas disease, caused by the protozoan parasite Trypanosoma cruzi transmitted by blood-sucking insects of the subfamily Triatominae, is a major neglected tropical disease affecting 6 to 7 million of people worldwide. Rhodnius prolixus, one of the most important vectors of Chagas disease in Latin America, is known to be highly sensitive to environmental factors, including temperature. This study aimed to investigate the effects of different temperatures on R. prolixus development and life-cycle, its relationship with T. cruzi, and to gather information about the nutritional habits and energy consumption of R. prolixus. We exposed uninfected and infected R. prolixus to four different temperatures ranging from 24°C to 30°C, and monitored their survival, developmental rate, body and blood meal masses, urine production, and the temporal dynamics of parasite concentration in the excreted urine of the triatomines over the course of their development. Our results demonstrate that temperature significantly impacts R. prolixus development, life-cycle and their relationship with T. cruzi, as R. prolixus exposed to higher temperatures had a shorter developmental time and a higher mortality rate compared to those exposed to lower temperatures, as well as a lower ability to retain weight between blood meals. Infection also decreased the capacity of the triatomines to retain weight gained by blood-feeding to the next developmental stage, and this effect was proportional to parasite concentration in excreted urine. We also showed that T. cruzi multiplication varied depending on temperature, with the lowest temperature having the lowest parasite load. Our findings provide important insights into the potential impact of climate change on the epidemiology of Chagas disease, and can contribute to efforts to model the future distribution of this disease. Our study also raises new questions, highlighting the need for further research in order to understand the complex interactions between temperature, vector biology, and parasite transmission.

MeSH terms

  • Animals
  • Chagas Disease* / parasitology
  • Humans
  • Insect Vectors / parasitology
  • Life Cycle Stages
  • Parasite Load
  • Rhodnius* / parasitology
  • Temperature
  • Trypanosoma cruzi*

Grants and funding

This work was made possible thanks to the Calmette & Yersin doctoral grant from the Department of International Affairs of the Institut Pasteur awarded to HL. AAG was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) productivity grant [grant number 304862/2022-3]. The research costs necessary for this work were funded by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais, FAPEMIG [grant number PPM-00162-17], the Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, INCTEM/CNPq [grant number 465678/2014-9] awarded to AAG, and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001, as general support of this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.