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

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.

[1]  R. Ignell,et al.  Dengue infection modulates locomotion and host seeking in Aedes aegypti , 2020, PLoS neglected tropical diseases.

[2]  C. Botto-Mahan,et al.  Trypanosoma cruzi could affect wild triatomine approaching behaviour to humans by altering vector nutritional status: a field test. , 2020, Acta tropica.

[3]  M. Lorenzo,et al.  Species-specific patterns of shelter exploitation in Chagas disease vectors of the genus Rhodnius. , 2020, Acta tropica.

[4]  A. Guarneri Infecting Triatomines with Trypanosomes. , 2020, Methods in molecular biology.

[5]  M. Lorenzo,et al.  Activity and shelter-related behavior in Rhodnius prolixus: The role of host odours. , 2019, Acta tropica.

[6]  W. Monteiro,et al.  Oral Transmission of Trypanosoma cruzi, Brazilian Amazon , 2019, Emerging infectious diseases.

[7]  A. L. R. Roque,et al.  Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil , 2018, Parasites & Vectors.

[8]  R. Herbison Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation , 2017, Front. Ecol. Evol..

[9]  V. Soccol,et al.  Recently differentiated epimastigotes from Trypanosoma cruzi are infective to the mammalian host , 2017, Molecular microbiology.

[10]  M. Lorenzo,et al.  Colonization of Rhodnius prolixus gut by Trypanosoma cruzi involves an extensive parasite killing , 2016, Parasitology.

[11]  D. Salmon,et al.  Monitoring of the Parasite Load in the Digestive Tract of Rhodnius prolixus by Combined qPCR Analysis and Imaging Techniques Provides New Insights into the Trypanosome Life Cycle , 2015, PLoS neglected tropical diseases.

[12]  A. Dobson,et al.  Rhodnius prolixus Life History Outcomes Differ when Infected with Different Trypanosoma cruzi I Strains. , 2015, The American journal of tropical medicine and hygiene.

[13]  J. M. Latorre-Estivalis,et al.  Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene , 2015, PLoS neglected tropical diseases.

[14]  A. Muñoz-Calderón,et al.  Update on oral Chagas disease outbreaks in Venezuela: epidemiological, clinical and diagnostic approaches , 2015, Memorias do Instituto Oswaldo Cruz.

[15]  M. Lorenzo,et al.  Trypanosoma cruzi, Etiological Agent of Chagas Disease, Is Virulent to Its Triatomine Vector Rhodnius prolixus in a Temperature-Dependent Manner , 2015, PLoS neglected tropical diseases.

[16]  O. DeSouza,et al.  Molecular basis of peripheral olfactory plasticity in Rhodnius prolixus, a Chagas disease vector , 2015, Front. Ecol. Evol..

[17]  M. Lorenzo,et al.  Effects of Infection by Trypanosoma cruzi and Trypanosoma rangeli on the Reproductive Performance of the Vector Rhodnius prolixus , 2014, PloS one.

[18]  P. Nouvellet,et al.  The Improbable Transmission of Trypanosoma cruzi to Human: The Missing Link in the Dynamics and Control of Chagas Disease , 2013, PLoS neglected tropical diseases.

[19]  V. Ros,et al.  Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour , 2013, Molecular ecology.

[20]  Meir Shillor,et al.  A Model for Chagas Disease with Oral and Congenital Transmission , 2013, PloS one.

[21]  F. Thomas,et al.  Evolutionary routes leading to host manipulation by parasites , 2012 .

[22]  M. Shikanai-Yasuda,et al.  Oral transmission of Chagas disease. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[23]  F. Thomas,et al.  Host manipulation by parasites: a multidimensional phenomenon , 2010 .

[24]  C. Botto-Mahan Trypanosoma cruzi induces life-history trait changes in the wild kissing bug Mepraia spinolai: implications for parasite transmission. , 2009, Vector borne and zoonotic diseases.

[25]  Clément Vinauger,et al.  Behavioural and physiological state dependency of host seeking in the blood-sucking insect Rhodnius prolixus , 2009, Journal of Experimental Biology.

[26]  U. Kitron,et al.  Strong Host-Feeding Preferences of the Vector Triatoma infestans Modified by Vector Density: Implications for the Epidemiology of Chagas Disease , 2009, PLoS neglected tropical diseases.

[27]  R. Barrozo,et al.  Temporal modulation and adaptive control of the behavioural response to odours in Rhodnius prolixus. , 2008, Journal of insect physiology.

[28]  U. Kitron,et al.  Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina , 2006, Parasitology.

[29]  C. Botto-Mahan,et al.  Chagas disease parasite induces behavioural changes in the kissing bug Mepraia spinolai. , 2006, Acta tropica.

[30]  R. Gürtler,et al.  Chagas disease control: deltamethrin-treated collars reduce Triatoma infestans feeding success on dogs. , 2005, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[31]  H. Hurd Manipulation of medically important insect vectors by their parasites. , 2003, Annual review of entomology.

[32]  R. Gürtler,et al.  Effects of refuge availability on the population dynamics of Triatoma infestans in central Argentina , 2003 .

[33]  C. Wisnivesky-Colli,et al.  Probability of Trypanosoma cruzi transmission by Triatoma infestans (Hemiptera: Reduviidae) to the opossum Didelphis albiventris (Marsupialia: Didelphidae). , 2001, The American journal of tropical medicine and hygiene.

[34]  M. Lorenzo,et al.  Activity pattern in relation to refuge exploitation and feeding in Triatoma infestans (Hemiptera: Reduviidae). , 1998, Acta tropica.

[35]  M. Lorenzo,et al.  The spatial pattern of defaecation in Triatoma infestans and the role of faeces as a chemical mark of the refuge , 1996 .

[36]  D. Hoft,et al.  Gastric invasion by Trypanosoma cruzi and induction of protective mucosal immune responses , 1996, Infection and immunity.

[37]  S. Catalá,et al.  Development of Trypanosoma cruzi in Triatoma infestans: influence of temperature and blood consumption. , 1995, The Journal of parasitology.

[38]  M. M. Lima,et al.  Development and Reproduction of Panstrongylus megistus (Hemiptera: Reduviidae) Infected with Trypanosoma cruzi, Under Laboratory Conditions , 1992 .

[39]  G. Schaub,et al.  Parasite/host-interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: influence of starvation of the bug. , 1989, Annals of tropical medicine and parasitology.