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

Abstract

BackgroundAs 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 FindingsIn 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/SignificanceWe 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.

Evolutionary ecology of Chagas disease; what do we know and what do we need?

“…Hypothetically, different strains could thus be transmitted with different efficacies if they had different capacities in manipulating (or at least affecting) their vector's behaviour. In the last few years, T. cruzi has indeed been shown to affect the dispersal of T. dimidiata (Nouvellet, Ramirez‐Sierra, Dumonteil, & Gourbière, ; Ramirez‐Sierra, Herrera‐Aguilar, Gourbière, & Dumonteil, ) and R. prolixus (Marlière et al., ). Even more intriguingly, infected bugs have been shown to bite 45% more often than uninfected individuals, and the time before defecation to be reduced by 30% by infection (Botto‐Mahan, Cattan, & Medel, ).…”

Effects of the infection with Trypanosoma cruzi on the feeding and excretion/defecation patterns of Triatoma infestans

“…The results of many of these studies led to establish the convention that T. cruzi is not pathogenic for their insect vectors, although the term 'sub-pathogenic' was proposed for this species since some effects may occur if there is a stressor present (Schaub, 2009). However, in recent years the effects of T. cruzi on survival, post-embryonic development, behavior and different physiological processes in different species of triatomines have been described (Eichler & Schaub, 2002;Botto-Mahan et al, 2006Schaub, 2006Schaub, , 2009Vallejo et al, 2009;Oliveira et al, 2010;Fellet et al, 2014;Elliot et al, 2015;Marliére et al, 2015).…”

Alteration of the social and spatial organization of the vector of Chagas disease,Triatoma infestans, by the parasiteTrypanosoma cruzi

“…In R. pallescens, T. cruzi infection did not significantly impact flight initiation, but it was observed that infected females flew significantly faster than males from 30 s to 2 min after flight initiation 41 . The locomotory activity of R. prolixus was decreased by infection: the total number of movements was 20% less than that observed in non-infected insects 42 . The time to find a host for an infected M. spinolai was almost twice as fast as for a non-infected insect 33 .…”

“…Ramirez-Sierra et al (2010) have already reported an increase of the dispersion on the field of infected females of T. dimidiata 39 . Infected nymphs of R. prolixus exhibited, on the contrary, a reduction of their locomotory activity 42 .…”