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

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

Revisiting Trypanosoma rangeli Transmission Involving Susceptible and Non-Susceptible Hosts

Submitted by Nuzia Santos ([email protected]) on 2016-03-11T17:02:01Z No. of bitstreams: 1 Revisiting Trypanosoma rangeli Transmission Involving Susceptible and Non-Susceptible Hosts.pdf: 438567 bytes, checksum: ad700ae3da5ea0d4deba26067403c799 (MD5)Approved for entry into archive by Nuzia Santos ([email protected]) on 2016-03-11T17:16:51Z (GMT) No. of bitstreams: 1 Revisiting Trypanosoma rangeli Transmission Involving Susceptible and Non-Susceptible Hosts.pdf: 438567 bytes, checksum: ad700ae3da5ea0d4deba26067403c799 (MD5)Made available in DSpace on 2016-03-11T17:16:51Z (GMT). No. of bitstreams: 1 Revisiting Trypanosoma rangeli Transmission Involving Susceptible and Non-Susceptible Hosts.pdf: 438567 bytes, checksum: ad700ae3da5ea0d4deba26067403c799 (MD5) Previous issue date: 2015Fundação Oswaldo Cruz. Centro de Pesquisas René Rachou. Comportamento de Vetores e Interação com Patógenos. Belo Horizonte, MG, BrasilUniversidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Departamento de Parasitologia. Belo Horizonte, MG, BrasilFundação Oswaldo Cruz. Centro de Pesquisas René Rachou. Comportamento de Vetores e Interação com Patógenos. Belo Horizonte, MG, BrasilTrypanosoma rangeli infects several triatomine and mammal species in South America. Its transmission is known to occur when a healthy insect feeds on an infected mammal or when an infected insect bites a healthy mammal. In the present study we evaluated the classic way of T. rangeli transmission started by the bite of a single infected triatomine, as well as alternative ways of circulation of this parasite among invertebrate hosts. The number of metacyclic trypomastigotes eliminated from salivary glands during a blood meal was quantified for unfed and recently fed nymphs. The quantification showed that ~50,000 parasites can be liberated during a single blood meal. The transmission of T. rangeli from mice to R. prolixus was evaluated using infections started through the bite of a single infected nymph. The mice that served as the blood source for single infected nymphs showed a high percentage of infection and efficiently transmitted the infection to new insects. Parasites were recovered by xenodiagnosis in insects fed on mice with infections that lasted approximately four months. Hemolymphagy and co-feeding were tested to evaluate insect-insect T. rangeli transmission. T. rangeli was not transmitted during hemolymphagy. However, insects that had co-fed on mice with infected conspecifics exhibited infection rates of approximately 80%. Surprisingly, 16% of the recipient nymphs became infected when pigeons were used as hosts. Our results show that T. rangeli is efficiently transmitted between the evaluated hosts. Not only are the insect-mouse-insect transmission rates high, but parasites can also be transmitted between insects while co-feeding on a living host. We show for the first time that birds can be part of the T. rangeli transmission cycle as we proved that insect-insect transmission is feasible during a co-feeding on these hosts

Co-existing locomotory activity and gene expression profiles in a kissing-bug vector of Chagas disease

This is the accepted version of the following article: "Co-existing locomotory activity and gene expression profiles in a kissing-bug vector of Chagas disease", which has been published in final form at https://www.sciencedirect.com/science/article/pii/S0022191019304275?via%3DihubInternational audienceThe triatomine bug Rhodnius prolixus is a main vector of Chagas disease, which affects several million people in Latin-America. These nocturnal insects spend most of their locomotory activity during the first hours of the scotophase searching for suitable hosts. In this study we used multivariate analysis to characterize spontaneous locomotory activity profiles presented by 5th instar nymphs. In addition, we investigated whether sex and the expression of the foraging (Rpfor) gene could modulate this behavioral trait. Hierarchical Clustering and Redundancy Analyses detected individuals with distinct locomotory profiles. In addition to a great variation in locomotory intensity, we found that a proportion of nymphs walked during unusual time intervals. Locomotory activity profiles were mostly affected by the cumulative activity expressed by the nymphs. These effects promoted by cumulative activity were in turn influenced by nymph sex. Sex and the Rpfor expression had a significant influence on the profiles, as well as in the levels of total activity. In conclusion, the locomotory profiles evinced by the multivariate analyses suggest the co-existence of different foraging strategies in bugs. Additionally, we report sex-specific effects on the locomotion patterns of 5th instar R. prolixus, which are apparently modulated by the differential expression of the Rpfor gene

Effects of Infection by Trypanosoma cruzi and Trypanosoma rangeli on the Reproductive Performance of the Vector Rhodnius prolixus

Submitted by Nuzia Santos ([email protected]) on 2015-03-17T16:24:54Z No. of bitstreams: 1 2014_154.pdf: 572927 bytes, checksum: 44205268319c337d2440181fadb5c023 (MD5)Approved for entry into archive by Nuzia Santos ([email protected]) on 2015-03-17T16:25:01Z (GMT) No. of bitstreams: 1 2014_154.pdf: 572927 bytes, checksum: 44205268319c337d2440181fadb5c023 (MD5)Approved for entry into archive by Nuzia Santos ([email protected]) on 2015-03-17T16:27:48Z (GMT) No. of bitstreams: 1 2014_154.pdf: 572927 bytes, checksum: 44205268319c337d2440181fadb5c023 (MD5)Made available in DSpace on 2015-03-17T16:27:48Z (GMT). No. of bitstreams: 1 2014_154.pdf: 572927 bytes, checksum: 44205268319c337d2440181fadb5c023 (MD5) Previous issue date: 2014Fundação Oswaldo Cruz. Centro de Pesquisas Rene Rachou. Comportamento de Vetores e Interação com Patógenos. Belo Horizonte, MG, BrasilFundação Oswaldo Cruz. Centro de Pesquisas Rene Rachou. Comportamento de Vetores e Interação com Patógenos. Belo Horizonte, MG, BrasilUniversidade Federal de Viçosa. Departamento de Entomologia. Viçosa, MG, BrazilSwedish University of Agricultural Sciences. Unit of Chemical Ecology. Department of Plant Protection Biology. Alnarp, SwedenFundação Oswaldo Cruz. Centro de Pesquisas Rene Rachou. Comportamento de Vetores e Interação com Patógenos. Belo Horizonte, MG, BrasilThe insect Rhodnius prolixus is responsible for the transmission of Trypanosoma cruzi, which is the etiological agent of Chagas disease in areas of Central and South America. Besides this, it can be infected by other trypanosomes such as Trypanosoma rangeli. The effects of these parasites on vectors are poorly understood and are often controversial so here we focussed on possible negative effects of these parasites on the reproductive performance of R. prolixus, specifically comparing infected and uninfected couples. While T. cruzi infection did not delay pre-oviposition time of infected couples at either temperature tested (25 and 30uC) it did, at 25uC, increase the e-value in the second reproductive cycle, as well as hatching rates. Meanwhile, at 30uC, T. cruzi infection decreased the e-value of insects during the first cycle and also the fertility of older insects. When couples were instead infected with T. rangeli, pre-oviposition time was delayed, while reductions in the e-value and hatching rate were observed in the second and third cycles. We conclude that both T. cruzi and T. rangeli can impair reproductive performance of R. prolixus, although for T. cruzi, this is dependent on rearing temperature and insect age. We discuss these reproductive costs in terms of potential consequences on triatomine behavior and survival

Number of parasites found in the intestinal tract of <i>T</i>. <i>rangeli</i>-infected <i>R</i>. <i>prolixus</i> 5^th instar nymphs that were fed on mice at different stages of infection.

<p>The horizontal lines represent the median value obtained for each group.</p

Infection rates of <i>R</i>. <i>prolixus</i> 5^th instar nymphs that fed on <i>T</i>. <i>rangeli-</i>infected mice on different days after infection.

<p>The data shown represent the mean of three biological replicates, except from the data for 126 days post infection, which are based on a single experiment using five tested insects. For the other replicates, 25–30 nymphs were used for each evaluation day.</p

Complement-mediated <i>T</i>. <i>rangeli</i> metacyclic trypomastigote lysis by mouse and pigeon serum.

<p>Data are presented as the percentage of lysed trypomastigotes after 30 min of incubation whit non-heat inactivated serum (n = 3).</p

Estimation of the parasite load present in the salivary gland (SG) of starved and fed 5^th instar nymphs of <i>R</i>. <i>prolixus</i> 45 days after infection by <i>T</i>. <i>rangeli</i> (parasites—Neubauer chamber and RNA-Cl1 sno gene copies/μL—qPCR).

<p>Values correspond to means ± SE.</p