Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene

PLoS Negl Trop Dis. 2015 Aug 20;9(8):e0003973. doi: 10.1371/journal.pntd.0003973. eCollection 2015.

Abstract

Background: As a result of evolution, the biology of triatomines must have been significantly adapted to accommodate trypanosome infection in a complex network of vector-vertebrate-parasite interactions. Arthropod-borne parasites have probably developed mechanisms, largely still unknown, to exploit the vector-vertebrate host interactions to ensure their transmission to suitable hosts. Triatomines exhibit a strong negative phototaxis and nocturnal activity, believed to be important for insect survival against its predators.

Methodology/principal findings: In this study we quantified phototaxis and locomotion in starved fifth instar nymphs of Rhodnius prolixus infected with Trypanosoma cruzi or Trypanosoma rangeli. T. cruzi infection did not alter insect phototaxis, but induced an overall 20% decrease in the number of bug locomotory events. Furthermore, the significant differences induced by this parasite were concentrated at the beginning of the scotophase. Conversely, T. rangeli modified both behaviors, as it significantly decreased bug negative phototaxis, while it induced a 23% increase in the number of locomotory events in infected bugs. In this case, the significant effects were observed during the photophase. We also investigated the expression of Rpfor, the triatomine ortholog of the foraging gene known to modulate locomotion in other insects, and found a 4.8 fold increase for T. rangeli infected insects.

Conclusions/significance: We demonstrated for the first time that trypanosome infection modulates the locomotory activity of the invertebrate host. T. rangeli infection seems to be more broadly effective, as besides affecting the intensity of locomotion this parasite also diminished negative phototaxis and the expression of a behavior-associated gene in the triatomine vector.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Behavior, Animal*
  • Gene Expression Regulation*
  • Host-Parasite Interactions
  • Insect Proteins / genetics
  • Insect Proteins / metabolism
  • Insect Vectors / genetics
  • Insect Vectors / parasitology*
  • Insect Vectors / physiology
  • Light
  • Molecular Sequence Data
  • Motor Activity* / genetics
  • Rhodnius / genetics
  • Rhodnius / parasitology*
  • Rhodnius / physiology
  • Trypanosoma / physiology*
  • Trypanosoma cruzi / physiology
  • Trypanosoma rangeli / physiology

Substances

  • Insect Proteins

Grants and funding

MGL was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico productivity grants (306586/2012-6). This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (441999/2014-0), Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (573959/2008-0), Programa Estratégico de Apoio a Pesquisa em Saúde VI/FIOCRUZ (407614/2012-5), and Programa de Excelência em Pesquisa 401973/2012-3. This research was funded in part by NSERC (RPG261940) and the Canada Research Chairs program (CL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.