1921
Volume 93, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

The effect of a parasite on the life history of its vector is important for understanding and predicting disease transmission. Chagas disease agent is a generalist parasite that is diverse across scales from its genetic diversity to the 100s of mammal and vector species it infects. Its vertebrate hosts show quite variable responses to infection, however, to date there are no studies looking at how variability might result in variable outcomes in its invertebrate host. Therefore, we investigated the effect of different I strains on survival and development. We found significant variation between insects infected with different strains, with some strains having no effect, as compared with uninfected insects, and others with significantly lower survival and development. We also found that different variables had varying importance between strains, with the effect of time postinfection and the blood:weight ratio of the infective meal significantly affecting the survival of insects infected with some strains, but not others. Our results suggest that can be pathogenic not only to its vertebrate hosts but also to its invertebrate hosts.

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2015-09-02
2017-11-18
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References

  1. Rassi A, Jr Rassi A, Marin-Neto JA, , 2010. Chagas disease. Lancet 375: 13881402.[Crossref]
  2. World Health Organization, 2015. Chagas disease in Latin America: epidemiological update based on the 2010 estimates. Weekly Epidemiological Record 90: 3344.
  3. WHO Expert Committee on the Control of Chagas Disease (2000: Brasilia, Brazil) Control of Chagas disease: second report of the WHO expert committee. WHO Technical Report Series 905: 1106.
  4. Devera R, Fernandes O, Coura JR, , 2003. Should Trypanosoma cruzi be called “cruzi” complex? A review of the parasite diversity and the potential of selecting population after in vitro culturing and mice infection. Mem Inst Oswaldo Cruz 98: 112.[Crossref]
  5. Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM, Teixeira MMG, Schijman AG, Llewellyn MS, Lages-Silva E, Machado CR, Andrade SG, Sturm NR, , 2012. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol 12: 240253.[Crossref]
  6. Yeo M, Acosta N, Llewellyn M, Sánchez H, Adamson S, Miles GA, López E, González N, Patterson JS, Gaunt MW, de Arias AR, Miles MA, , 2005. Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. Int J Parasitol 35: 225233.[Crossref]
  7. Llewellyn MS, Miles MA, Carrasco HJ, Lewis MD, Yeo M, Vargas J, Torrico F, Diosque P, Valente V, Valente SA, Gaunt MW, , 2009. Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog 5: e1000410.[Crossref]
  8. Macedo AM, Machado CR, Oliveira RP, Pena SDJ, , 2004. Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of chagas disease. Mem Inst Oswaldo Cruz 99: 112. Available at: http://www.ncbi.nlm.nih.gov/pubmed/15057339.[Crossref]
  9. Mejía-Jaramillo AM, Peña VH, Triana-Chávez O, , 2009. Trypanosoma cruzi: biological characterization of lineages I and II supports the predominance of lineage I in Colombia. Exp Parasitol 121: 8391.[Crossref]
  10. Bahia MT, Tafuri WL, Caliari MV, Veloso VM, Carneiro CM, Coelho GLLM, de Lana M, , 2002. Comparison of Trypanosoma cruzi infection in dogs inoculated with blood or metacyclic trypomastigotes of Berenice-62 and Berenice-78 strains via intraperitoneal and conjunctival routes. Rev Soc Bras Med Trop 35: 339345. Available at: http://www.ncbi.nlm.nih.gov/pubmed/12170329.[Crossref]
  11. Deane MP, Lenzi HL, Jansen A, , 1984. Trypanosoma cruzi: vertebrate and invertebrate cycles in the same mammal host, the opossum Didelphis marsupialis . Mem Inst Oswaldo Cruz 79: 513515.[Crossref]
  12. Jansen A, Roque ALR, Telleria J, Tibayrenc M, , 2010. Domestic and wild mammalian reservoirs. , eds. American Trypanosomiasis Chagas Disease. Amsterdam, The Netherlands: Elsevier, 249276.[Crossref]
  13. Teixeira ARL, Nascimento RJ, Sturm NR, , 2006. Evolution and pathology in Chagas disease-a review. Mem Inst Oswaldo Cruz 101: 463491. Available at: http://www.ncbi.nlm.nih.gov/pubmed/17072450.[Crossref]
  14. Garnham P, , 1955. The comparative pathogenicity of Protozoa in their vertebrate and invertebrate hosts. Symp Soc Gen Microbiol 5: 191206.
  15. Schaub GA, , 1989. Does Trypanosoma cruzi stress its vectors? Parasitol Today 5: 185188.[Crossref]
  16. Schaub GA, , 1992. The effects of trypanosomatids on insects. Adv Parasitol 31: 255319. Available at: http://www.ncbi.nlm.nih.gov/pubmed/1496928.[Crossref]
  17. Schaub GA, , 1994. Pathogenicity of trypanosomatids on insects. Parasitol Today 10: 463468.[Crossref]
  18. Schaub GA, Meiser CK, Balczun C, Mehlhorn H, , 2011. Interactions of Trypanosoma cruzi and Triatomines. , ed. Progress in Parasitology. Berlin, Heidelberg: Springer Berlin Heidelberg, 155178.[Crossref]
  19. Vallejo GA, Guhl F, Schaub GA, , 2009. Triatominae-Trypanosoma cruzi/T. rangeli: vector-parasite interactions. Acta Trop 110: 137147.[Crossref]
  20. Schaub GA, Simpson SJ, Casas J, , 2009. Interactions of trypanosomatids and triatomines. , eds. Advances in Insect Physiology, Volume 37. Burlington, VT: Academic Press, 177242.
  21. Schaub GA, , 1988. Development of isolated and group-reared first instars of Triatoma infestans infected with Trypanosoma cruzi . Parasitol Res 74: 593594.[Crossref]
  22. Schaub GA, Lösch P, , 1988. Trypanosoma cruzi: origin of metacyclic trypomastigotes in the urine of the vector Triatoma infestans . Exp Parasitol 65: 174186. Available at: http://www.ncbi.nlm.nih.gov/pubmed/3280333.[Crossref]
  23. Schaub G, , 1988. Developmental time and mortality of larvae of Triatoma infestans infected with Trypanosoma cruzi . Trans R Soc Trop Med Hyg 82: 9496.[Crossref]
  24. Kollien A, Schaub G, , 1998. The development of Trypanosoma cruzi (Trypanosomatidae) in the Reduviid bug Triatoma infestans (Insecta): influence of starvation. J Eukaryot Microbiol 45: 5963.[Crossref]
  25. Kollien AH, Schmidt J, Schaub GA, , 1998. Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans . Acta Trop 70: 127141.[Crossref]
  26. Kollien A, Schaub G, , 1998. Trypanosoma cruzi in the rectum of the bug Triatoma infestans: effects of blood ingestion by the starved vector. Am J Trop Med Hyg 59: 166170.
  27. Schaub GA, Losch P, , 1989. Parasite/host-interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: influence of starvation on the bug. Ann Trop Med Parasitol 83: 215223.[Crossref]
  28. Botto-Mahan C, Cattan PE, Medel R, , 2006. Chagas disease parasite induces behavioural changes in the kissing bug Mepraia spinolai . Acta Trop 98: 219223.[Crossref]
  29. Botto-Mahan C, Ossa CG, Medel R, , 2008. Direct and indirect pathways of fitness-impact in a protozoan-infected kissing bug. Physiol Entomol 33: 2530.[Crossref]
  30. Botto-Mahan C, , 2009. Trypanosoma cruzi induces life-history trait changes in the wild kissing bug Mepraia spinolai: implications for parasite transmission. Vector Borne Zoonotic Dis 9: 505510.[Crossref]
  31. Lima MM, Borges-Pereira J, Albuquerque Dos Santos JA, Teixeira Pinto Z, Vianna Braga M, , 1992. Development and reproduction of Panstrongylus megistus (Hemiptera: Reduviidae) infected with Trypanosoma cruzi, under laboratory conditions. Ann Entomol Soc Am 85: 458461.[Crossref]
  32. Neves D, Peres R, , 1975. Aspectos da biologia do Rhodnius prolixus quando alimentado em animais sadios ou infectados com o Trypanosoma cruzi . Rev Bras Biol 35: 317320.
  33. Dos Santos JR, Lacombe D, , 1985. Estudos relativos a duracao da ecdise e oviposicao de Triatoma infestans infectado pelo Trypanosoma cruzi . An Acad Bras Cienc 57: 127.
  34. Watkins R, , 1969. Host-parasite interaction between Trypanosoma species and Rhodnius prolixus Stal (Hemiptera, Reduviidae). Ph.D. Thesis, University of California, Berkeley.
  35. Oliveira TG, Carvalho-Costa FA, Gomes TF, Sarquis O, Sposina R, Lima MM, , 2010. Developmental and reproductive patterns of Triatoma brasiliensis infected with Trypanosoma cruzi under laboratory conditions. Mem Inst Oswaldo Cruz 105: 10571060. Available at: http://www.ncbi.nlm.nih.gov/pubmed/21225206.[Crossref]
  36. Cura CI, Mejía-Jaramillo AM, Duffy T, Burgos JM, Rodriguero M, Cardinal MV, Kjos S, Gurgel-Gonçalves R, Blanchet D, De Pablos LM, Tomasini N, da Silva A, Russomando G, Cuba Cuba C, Aznar C, Abate T, Levin MJ, Osuna A, Gürtler RE, Diosque P, Solari A, Triana-Chávez O, Schijman AG, , 2010. Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. Int J Parasitol 40: 15991607.[Crossref]
  37. Mejía-Jaramillo AM, Arboleda-Sánchez S, Rodríguez IB, Cura C, Salazar A, Del Mazo J, Triana-Chávez O, Schijman AG, , 2009. Geographical clustering of Trypanosoma cruzi I groups from Colombia revealed by low-stringency single specific primer-PCR of the intergenic regions of spliced-leader genes. Parasitol Res 104: 399410.[Crossref]
  38. Jaramillo N, Moreno J, Triana O, Arcos-Burgos M, Muñoz S, Solari A, , 1999. Genetic structure and phylogenetic relationships of Colombian Trypanosoma cruzi populations as determined by schizodeme and isoenzyme markers. Am J Trop Med Hyg 61: 986993. Available at: http://www.ncbi.nlm.nih.gov/pubmed/10674683.
  39. Olmo F, Escobedo-Orteg J, Palma P, Sánchez-Moreno M, Mejía-Jaramillo A, Triana O, Marín C, , 2014. Specific primers design based on the superoxide dismutase b gene for Trypanosoma cruzi as a screening tool: validation method using strains from Colombia classified according to their discrete typing unit. Asian Pac J Trop Med 7: 854859.[Crossref]
  40. Falla A, Herrera C, Fajardo A, Montilla M, Vallejo GA, Guhl F, , 2009. Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Trop 110: 1521.[Crossref]
  41. Gaunt M, Miles M, , 2000. The ecotopes and evolution of triatomine bugs (triatominae) and their associated trypanosomes. Mem Inst Oswaldo Cruz 95: 557565.[Crossref]
  42. Carrasco HJ, Frame IA, Valente SA, Miles MA, , 1996. Genetic exchange as a possible source of genomic diversity in sylvatic populations of Trypanosoma cruzi . Am J Trop Med Hyg 54: 418424.
  43. Lewis MD, Ma J, Yeo M, Carrasco HJ, Llewellyn MS, Miles MA, , 2009. Genotyping of Trypanosoma cruzi: systematic selection of assays allowing rapid and accurate discrimination of all known lineages. Am J Trop Med Hyg 81: 10411049.[Crossref]
  44. Fellet MR, Lorenzo MG, Elliot SL, Carrasco D, Guarneri AA, , 2014. Effects of Infection by Trypanosoma cruzi and Trypanosoma rangeli on the reproductive performance of the vector Rhodnius prolixus . PLoS One 9: e105255.[Crossref]
  45. Ferreira LL, Lorenzo MG, Elliot SL, Guarneri AA, , 2010. A standardizable protocol for infection of Rhodnius prolixus with Trypanosoma rangeli, which mimics natural infections and reveals physiological effects of infection upon the insect. J Invertebr Pathol 105: 9197.[Crossref]
  46. Castro LA, Peterson JK, Saldaña A, Perea MY, Calzada JE, Pineda V, Dobson AP, Gottdenker NL, , 2014. Flight behavior and performance of Rhodnius pallescens (Hemiptera: Reduviidae) on a tethered flight mill. J Med Entomol 51: 10101018.[Crossref]
  47. Whitten MM, Mello CB, Gomes SA, Nigam Y, Azambuja P, Garcia ES, Ratcliffe NA, , 2001. Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Exp Parasitol 98: 4457.[Crossref]
  48. Azambuja P, Feder D, Garcia ES, , 2004. Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Exp Parasitol 107: 8996.[Crossref]
  49. Cortez MR, Provençano A, Silva CE, Mello CB, Zimmermann LT, Schaub GA, Garcia ES, Azambuja P, Gonzalez MS, , 2012. Trypanosoma cruzi: effects of azadirachtin and ecdysone on the dynamic development in Rhodnius prolixus larvae. Exp Parasitol 131: 363371.[Crossref]
  50. Mello CB, Azambuja P, Garcia ES, Ratcliffe NA, , 1996. Differential in vitro and in vivo behavior of three strains of Trypanosoma cruzi in the gut and hemolymph of Rhodnius prolixus . Exp Parasitol 82: 112121.[Crossref]
  51. Mello CB, Garcia E, Ratcliffe NA, Azambuja P, , 1995. Trypaonsoma cruzi and Trypanosoma rangeli: interplay with hemolymph components of Rhodius prolixus . J Invertebr Pathol 65: 261268.[Crossref]
  52. Gaunt M, Miles M, , 2000. The ecotopes and evolution of triatomine bugs (triatominae) and their associated trypanosomes. Mem Inst Oswaldo Cruz 95: 557565. Available at: http://www.ncbi.nlm.nih.gov/pubmed/10904415.[Crossref]
  53. Herrera C, Bargues MD, Fajardo A, Montilla M, Triana O, Vallejo GA, Guhl F, , 2007. Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infect Genet Evol 7: 535539.[Crossref]
  54. Araújo CAC, Cabello PH, Jansen AM, , 2007. Growth behaviour of two Trypanosoma cruzi strains in single and mixed infections: in vitro and in the intestinal tract of the blood-sucking bug, Triatoma brasiliensis . Acta Trop 101: 225231.[Crossref]
  55. Araújo CAC, Waniek PJ, Jansen AM, , 2014. TcI/TcII co-infection can enhance Trypanosoma cruzi growth in Rhodnius prolixus . Parasit Vectors 7: 94.[Crossref]
  56. Nogueira NFS, Gonzalez MS, Gomes JE, de Souza W, Garcia E, Azambuja P, Nohara LL, Almeida IC, Zingales B, Colli W, , 2007. Trypanosoma cruzi: involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus . Exp Parasitol 116: 120128.[Crossref]
  57. Castro DP, Moraes CS, Gonzalez MS, Ratcliffe NA, Azambuja P, Garcia ES, , 2012. Trypanosoma cruzi immune response modulation decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLoS One 7: e36591.[Crossref]
  58. Borges EC, Machado EMM, Garcia ES, Azambuja P, , 2006. Trypanosoma cruzi: effects of infection on cathepsin D activity in the midgut of Rhodnius prolixus . Exp Parasitol 112: 130133.[Crossref]
  59. Ratcliffe NA, Nigam YN, Mello CB, Garcia ES, Azambuja P, , 1996. Trypanosoma cruzi and erythrocyte agglutinins : a comparative study of occurrence and properties in the gut and hemolymph of Rhodnius prolixus . Exp Parasitol 83: 8393.[Crossref]
  60. Schaub GA, Grünfelder CG, Zimmermann D, Peters W, , 1989. Binding of lectin-gold conjugates by two Trypanosoma cruzi strains in ampullae and rectum of Triatoma infestans . Acta Trop 46: 291301. Available at: http://www.ncbi.nlm.nih.gov/pubmed/2575865.[Crossref]
  61. Bice DE, Zeledon R, , 1970. Comparison of infectivity of strains of Trypanosoma cruzi (Chagas, 1909). J Parasitol 56: 663670.[Crossref]
  62. Urdaneta-Morales S, Rueda IG, , 1977. A comparative study of the behavior of Venezuelan and Brazilian strains of Trypanosoma (Schizotrypanum) cruzi in the Venezuelan invertebrate host (Rhodnius prolixus). Rev Inst Med Trop Sao Paulo 19: 241250.
  63. Perlowagora-Szumlewicz A, Muller CA, , 1982. Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas disease. 1-Comparative xenodiagnosis with nine triatomine species of animals with acute infections by Trypanosoma cruzi . Mem Inst Oswaldo Cruz 77: 3753.[Crossref]
  64. Mac Cord JR, Jurberg P, Lima MM, , 1983. Marcacao individual de tratomineos para estudos comportamentais e ecologicos. Mem Inst Oswaldo Cruz 78: 473476.[Crossref]
  65. Henriques C, Castro DP, Gomes LHF, Garcia ES, De Souza W, , 2012. Bioluminescent imaging of Trypanosoma cruzi infection in Rhodnius prolixus . Parasit Vectors 5: 115.[Crossref]
  66. Garcia E, Subrahmanyam B, Muller T, Rembold H, , 1989. Absorption, storage, organ distribution, and excretion of dietary [22, 23-3H2] dihydroazadirachtin A in the blood-feeding bug Rhodnius prolixus . J Insect Physiol 35: 743748.[Crossref]
  67. Gonzalez MS, Souza MS, Garcia ES, Nogueira NFS, Mello CB, Cánepa GE, Bertotti S, Durante IM, Azambuja P, Buscaglia CA, , 2013. Trypanosoma cruzi TcSMUG L-surface mucins promote development and infectivity in the triatomine vector Rhodnius prolixus . PLoS Negl Trop Dis 7: e2552.[Crossref]
  68. Garcia E, Azambuja P, Crampton JM, Beard CB, Louis C, , 1997. Infection of triatomines with Trypanosoma cruzi . , eds. The Molecular Biology of Insect Disease Vectors: A Methods Manual. London: Chapman & Hall, 146155.[Crossref]
  69. Azambuja P, Garcia E, Crampton JM, Beard CB, Louis C, , 1997. Care and maintenance of Triatomine colonies. , eds. The Molecular Biology of Insect Disease Vectors: A Methods Manual. London: Chapman & Hall, 5664.[Crossref]
  70. Calzada JE, Pineda V, Montalvo E, Alvarez D, Santamaría AM, Samudio F, Bayard V, Cáceres L, Saldaña A, , 2006. Human trypanosome infection and the presence of intradomicile Rhodnius pallescens in the western border of the Panama Canal, Panama. Am J Trop Med Hyg 74: 762765. Available at: http://www.ncbi.nlm.nih.gov/pubmed/16687677.
  71. Moser DR, Kirchhoff LV, Donelson JE, , 1989. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J Clin Microbiol 27: 14771482.
  72. R Core Team, 2014. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.r-project.org/.
  73. Giraudoux P, , 2013. pgirmess: Data Analysis in Ecology. Available at: http://cran.r-project.org/package=pgirmess.
  74. Therneau T, , 2014. A Package for Survival Analysis in S. Available at: http://cran.r-project.org/package=survival.
  75. Therneau T, Grambsch P, , 2000. Modeling Survival Data: Extending the Cox Model. New York, NY: Springer.[Crossref]
  76. Harrington DP, Fleming TR, , 1982. A class of rank test procedures for censored survival data. Biometrika 69: 553566.[Crossref]
  77. Peto R, Peto J, , 1972. Asymptotically efficient rank invariant test procedures. J R Stat Soc 135: 185207.
  78. Holm S, , 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6: 6570.
  79. Cox DR, , 1972. Regression models and life-tables. J R Stat Soc 34: 187220.
  80. Venables WN, Ripley BD, , 2002. Modern Applied Statistics with S, 4th edition. New York, NY: Springer.[Crossref]
  81. Schaub GA, , 1989. Trypanosoma cruzi : quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans . Exp Parasitol 68: 260273.[Crossref]
  82. Azambuja P, Garcia ES, Ratcliffe NA, , 2005. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 21: 568572.[Crossref]
  83. Chowdury M, Fistein B, , 1986. Excretion of Trypanosoma cruzi by various stages of Rhodnius prolixus . Int J Parasitol 16: 353359.[Crossref]
  84. Wood SF, , 1954. Environmental temperature as a factor in development of Trypanosoma cruzi in Triatoma protracta . Exp Parasitol 3: 227233.[Crossref]
  85. Zafra G, Mantilla JC, Valadares HM, Macedo AM, González CI, , 2008. Evidence of Trypanosoma cruzi II infection in Colombian chagasic patients. Parasitol Res 103: 731734.[Crossref]
  86. Andrade SG, Campos RF, Castro Sobral KS, Magalhães JB, Pereira Guedes RS, Guerreiro ML, , 2006. Reinfections with strains of Trypanosoma cruzi, of different biodemes as a factor of aggravation of myocarditis and myositis in mice. Rev Soc Bras Med Trop 39: 18.[Crossref]
  87. Lima V, Mangia R, Carreira J, Marchevsky R, Jansen A, , 1999. Trypanosoma cruzi: correlations of biological aspects of the life cycle in mice and triatomines. Mem Inst Oswaldo Cruz 94: 397402. Available at: http://www.ncbi.nlm.nih.gov/pubmed/10348990.[Crossref]
  88. Noireau F, Diosque P, Jansen AM, , 2009. Trypanosoma cruzi: adaptation to its vectors and its hosts. Vet Res 40: 26.[Crossref]
  89. Rodrigues CM, Valadares HMS, Francisco AF, Arantes JM, Campos CF, Teixeira-Carvalho A, Martins-Filho OA, Araujo MSS, Arantes RME, Chiari E, Franco GR, Machado CR, Pena SDJ, Faria AMC, Macedo AM, , 2010. Coinfection with different Trypanosoma cruzi strains interferes with the host immune response to infection. PLoS Negl Trop Dis 4: e846.[Crossref]
  90. Andrade LO, Machado CR, Chiari E, Pena SD, Macedo AM, , 1999. Differential tissue distribution of diverse clones of Trypanosoma cruzi in infected mice. Mol Biochem Parasitol 100: 163172. Available at: http://www.ncbi.nlm.nih.gov/pubmed/10391378.[Crossref]
  91. Tableman M, Sung Kim J, , 2005. Survival Analysis Using S. Boca Raton, FL: Chapman and Hall/CRC.
  92. Brener Z, , 1973. Biology of Trypanosoma cruzi . Annu Rev Microbiol 27: 347382.[Crossref]
  93. Aron J, May RM, Anderson RA, , 1982. The population dynamics of malaria. In: , editor. The Population Dynamics of Infectious Diseases: Theory and Applications. London: Chapman and Hall, 139179.[Crossref]
  94. Dobson A, , 2004. Population dynamics of pathogens with multiple host species. Am Nat 164 (Suppl 5): S64S78.[Crossref]
  95. Rohani P, Green CJ, Mantilla-Beniers NB, Grenfell BT, , 2003. Ecological interference between fatal diseases. Nature 422: 885888.[Crossref]
  96. Ferguson HM, Mackinnon MJ, Chan BH, Read AF, , 2003. Mosquito mortality and the evolution of malaria virulence. Evolution 57: 27922804. Available at: http://www.ncbi.nlm.nih.gov/pubmed/14761058.[Crossref]
  97. Peacock L, Ferris V, Bailey M, Gibson W, , 2007. Dynamics of infection and competition between two strains of Trypanosoma brucei brucei in the tsetse fly observed using fluorescent markers. Kinetoplastid Biol Dis 6: 4.[Crossref]
  98. Schaub GA, Eichler S, , 1998. The effects of aposymbiosis and of an infection with Blastocrithidia triatomae (Trypanosomatidae) on the tracheal system of the reduviid bugs Rhodnius prolixus and Triatoma infestans . J Insect Physiol 44: 131140. Available at: http://www.ncbi.nlm.nih.gov/pubmed/12769885.[Crossref]
  99. Eichler S, Schaub GA, , 2002. Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp Parasitol 100: 1727.[Crossref]
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  • Received : 19 Mar 2015
  • Accepted : 02 May 2015

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