The cost of being a killer’s accomplice: Trypanosoma cruzi impairs the fitness of kissing bugs

Cordero-Montoya, Gabino; Flores-Villegas, A. Laura; Salazar-Schettino, Paz Marı́a; Vences-Blanco, Mauro Omar; Rocha‐Ortega, Maya; Gutiérrez-Cabrera, Ana E.; Rojas-Ortega, Eréndira; Córdoba‐Aguilar, Alex

doi:10.1007/s00436-019-06413-8

Cited by 35 publications

(31 citation statements)

References 47 publications

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“…In contrast, pathogen infection can also lead to reduced lifespan and fecundity, as reported for Leishmania -infected sandflies [ 38 ], Cx. pipiens infected by the Rift Valley fever virus [ 39 ], and Trypanosoma -infected triatomine bugs [ 40 , 41 , 42 ], as examples of possible evolutionary arms races [ 27 ].…”

Section: Introductionmentioning

confidence: 99%

Pathogens Manipulating Tick Behavior—Through a Glass, Darkly

Benelli

2020

Pathogens

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Pathogens can manipulate the phenotypic traits of their hosts and vectors, maximizing their own fitness. Among the phenotypic traits that can be modified, manipulating vector behavior represents one of the most fascinating facets. How pathogens infection affects behavioral traits of key insect vectors has been extensively investigated. Major examples include Plasmodium, Leishmania and Trypanosoma spp. manipulating the behavior of mosquitoes, sand flies and kissing bugs, respectively. However, research on how pathogens can modify tick behavior is patchy. This review focuses on current knowledge about the behavioral changes triggered by Anaplasma, Borrelia, Babesia, Bartonella, Rickettsia and tick-borne encephalitis virus (TBEV) infection in tick vectors, analyzing their potential adaptive significance. As a general trend, being infected by Borrelia and TBEV boosts tick mobility (both questing and walking activity). Borrelia and Anaplasma infection magnifies Ixodes desiccation resistance, triggering physiological changes (Borrelia: higher fat reserves; Anaplasma: synthesis of heat shock proteins). Anaplasma infection also improves cold resistance in infected ticks through synthesis of an antifreeze glycoprotein. Being infected by Anaplasma, Borrelia and Babesia leads to increased tick survival. Borrelia, Babesia and Bartonella infection facilitates blood engorgement. In the last section, current challenges for future studies are outlined.

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Section: Introductionmentioning

confidence: 99%

Pathogens Manipulating Tick Behavior—Through a Glass, Darkly

Benelli

2020

Pathogens

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“…presence of trypomastigote forms in insects' excreta). Experimental infections of Mepraia pallidipennis from Morelos, Mexico, with two different strains of TcI-one from Morelos and another from Chilpancingo, Guerrero, Mexico, revealed that the parasite from the different geographic area (Chilpancingo) caused more debilitating effects on the vector, such as affecting their size and causing high parasitemia and low survival rate [24], thus evidencing possible role of genotype-by-genotype interactions [54] on triatomine populations and T. cruzi strains of the same geographical area. Hence, here we used a parasite (CL strain, TcVI) isolated from the excreta of field-captured T. infestans in Rio Grande do Sul, southern Brazil, same location where T. infestans and T. rubrovaria were collected, to ensure that the outcomes observed here were not caused by genotype impairments between vector population and parasite strain.…”

Section: Discussionmentioning

confidence: 99%

“…presence of trypomastigote forms in insects’ excreta). Experimental infections of Mepraia pallidipennis from Morelos, Mexico, with two different strains of TcI–one from Morelos and another from Chilpancingo, Guerrero, Mexico, revealed that the parasite from the different geographic area (Chilpancingo) caused more debilitating effects on the vector, such as affecting their size and causing high parasitemia and low survival rate [ 24 ], thus evidencing possible role of genotype-by-genotype interactions [ 54 ] on triatomine populations and T . cruzi strains of the same geographical area.…”

Section: Discussionmentioning

confidence: 99%

“…The effects of T . cruzi infection on triatomine behavior are scarcely investigated and the few studies available focused on fitness parameters, feeding-excretion behavior, aggregation/geotaxis and dispersion/locomotion (reviewed in [ 21 ],[ 58 ],[ 24 ],[ 29 ]). Feeding and excretion are behavioral parameters of paramount importance, since they determine the efficiency of T .…”

Section: Discussionmentioning

confidence: 99%

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Vector competence and feeding-excretion behavior of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) infected with Trypanosoma cruzi TcVI

et al. 2020

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Background Several studies addressed changes on the insect vector behavior due to parasite infection, but little is known for triatomine bugs, vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. We assessed infection rates and metacyclogenesis of T. cruzi (TcVI) in fifth-instar nymphs of Triatoma rubrovaria comparing with the primary vector Triatoma infestans. Also, biological parameters related to feeding-excretion behavior were evaluated aiming to identify which variables are most influenced by T. cruzi infection. Methodology/principal findings Fifth-instar nymphs of T. rubrovaria and T. infestans were fed on mice infected with T. cruzi (TcVI). We compared the presence and the number of parasite evolutive forms in excreta of both triatomine species at 30, 60 and 90 days post-infection (dpi) with traditional statistical analyses. Moreover, both species were analyzed through generalized linear models and multinomial logistic regression hypotheses for seven behavioral parameters related to hostseeking and feeding-excretion. Triatoma rubrovaria and T. infestans had similar overall infection and metacyclogenesis rates of T. cruzi TcVI in laboratory conditions. Regarding vector behavior, we confirmed that the triatomine's tendency is to move away from the bite region after a blood meal, probably to avoid being noticed by the vertebrate host. Interspecific differences were observed on the volume of blood ingested and on the proportion of individuals that excreted after the blood meal, revealing the higher feeding efficiency and dejection rates of T. infestans. The amount of ingested blood and the bite behavior of T.

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“…Moreover, Plasmodium falciparum increases fecundity and do not reduce survival in Anopheles gambiae (Alout et al, 2016). Evidence for cost of infection in other vector groups are less numerous; Trypanosoma cruzii infection decreases fecundity and survival of the triatomine bugs Meccus pallidipennis (Cordero-Montoya et al, 2019). Conflicting results regarding the manipulation of host choice by vector-borne parasites could result from differences in the associations of species tested (natural or not), as well as in the origin of the tested individuals, wild or laboratory-bred (Ferguson and Read, 2002;Tripet, 2009).…”

Section: Natural Versus Experimental Infectionsmentioning

confidence: 99%

Enhanced Attraction of Arthropod Vectors to Infected Vertebrates: A Review of Empirical Evidence

et al. 2020

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A large diversity of parasites manipulates their hosts in various ways to complete their own life cycle. Enhancing the attractiveness of their host to vectors has been suggested as a strategy allowing vector-borne parasites to increase their transmission. Indeed, a higher attraction of hematophagous, arthropod vectors to infected vertebrates compared to uninfected individuals has been found in many systems (e.g., Trypanosoma-tsetse flies, Leishmania-sand flies, Borrelia-ticks) but was most often verified in the Plasmodium-mosquitoes model. However, a number of studies found no difference in attractiveness, or a higher attractiveness of uninfected hosts. In this review, we present studies reporting a comparison of the attractiveness and/or the biting rate of infected and uninfected vertebrates. We then discuss several biological factors and experimental design aspects that can explain discrepancies between studies. Finally, we stress the importance of investigating the mechanisms of parasiteinduced increased attractiveness of infected hosts to conclude that such observations are cases of adaptive manipulation.

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The cost of being a killer’s accomplice: Trypanosoma cruzi impairs the fitness of kissing bugs

Cited by 35 publications

References 47 publications

Pathogens Manipulating Tick Behavior—Through a Glass, Darkly

Pathogens Manipulating Tick Behavior—Through a Glass, Darkly

Vector competence and feeding-excretion behavior of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) infected with Trypanosoma cruzi TcVI

Enhanced Attraction of Arthropod Vectors to Infected Vertebrates: A Review of Empirical Evidence

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