Stress dependent infection cost of the human malaria agent Plasmodium falciparum on its natural vector Anopheles coluzzii

Infection, Genetics and Evolution

Volumn 25, Issue , 2014, Pages 57-65

  Sangare, I ^a,b   Dabire, R ^a   Yameogo, B ^a   Da, D F ^a,b   Michalakis, Y ^b   Cohuet, A ^a,b  

^a Institut de Recherche en Sciences de la Santé   (Burkina Faso)

^b University de Montpellier   (France)

Author keywords

Environment; Infection cost; Malaria transmission; Mosquito fitness; Vector parasites interactions

Indexed keywords

SUGAR; GLUCOSE;

ANOPHELES; ANOPHELES COLUZZII; ARTICLE; BLOOD; CONTROLLED STUDY; ENVIRONMENTAL STRESS; FEEDING BEHAVIOR; FERTILITY; FITNESS; HOST PARASITE INTERACTION; LIFE HISTORY TRAIT; MEAL; NONHUMAN; NUTRIENT AVAILABILITY; PARASITE ISOLATION; PARASITE VECTOR; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SURVIVAL; ANIMAL; ANIMAL FOOD; CLASSIFICATION; DISEASE CARRIER; FEMALE; HUMAN; MALARIA FALCIPARUM; PARASITOLOGY; PHYSIOLOGY; REPRODUCTIVE FITNESS;

ANIMAL FEED; ANIMALS; ANOPHELES; BLOOD; FEMALE; FERTILITY; GENETIC FITNESS; GLUCOSE; HOST-PARASITE INTERACTIONS; HUMANS; INSECT VECTORS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; SURVIVAL ANALYSIS;

EID: 84899801375     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.04.006     Document Type: Article

References (77)

1. Aboagye-Antwi F., Guindo A., Traore A.S., Hurd H., Coulibaly M., Traore S., Tripet F. Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes. Malar. J. 2010, 9:243.
2. Afrane Y.A., Lawson B.W., Githeko A.K., Yan G. Effects of microclimatic changes caused by land use and land cover on duration of gonotrophic cycles of Anopheles gambiae (Diptera: Culicidae) in western Kenya highlands. J. Med. Entomol. 2005, 42:974-980.
3. Ahmed A.M., Hurd H. Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect. 2006, 8:308-315.
4. Akman-Anderson L., Olivier M., Luckhart S. Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infect. Immun. 2007, 75:4012-4019.
5. Anderson R.A., Knols B.G., Koella J.C. Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology 2000, 120:329-333.
6. Antonio-Nkondjio C., Awono-Ambene P., Toto J.C., Meunier J.Y., Zebaze-Kemleu S., Nyambam R., Wondji C.S., Tchuinkam T., Fontenille D. High malaria transmission intensity in a village close to Yaounde, the capital city of Cameroon. J. Med. Entomol. 2002, 39:350-355.
7. Arrighi R.B., Debierre-Grockiego F., Schwarz R.T., Faye I. The immunogenic properties of protozoan glycosylphosphatidylinositols in the mosquito Anopheles gambiae. Dev. Comp. Immunol. 2009, 33:216-223.
8. Boete C. Malaria parasites in mosquitoes: laboratory models, evolutionary temptation and the real world. Trends Parasitol. 2005, 21:445-447.
9. Boissiere A., Tchioffo M.T., Bachar D., Abate L., Marie A., Nsango S.E., Shahbazkia H.R., Awono-Ambene P.H., Levashina E.A., Christen R., Morlais I. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog. 2012, 8:e1002742.
10. Bousema T., Dinglasan R.R., Morlais I., Gouagna L.C., van Warmerdam T., Awono-Ambene P.H., Bonnet S., Diallo M., Coulibaly M., Tchuinkam T., Mulder B., Targett G., Drakeley C., Sutherland C., Robert V., Doumbo O., Toure Y., Graves P.M., Roeffen W., Sauerwein R., Birkett A., Locke E., Morin M., Wu Y., Churcher T.S. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS One 2012, 7:e42821.
11. Briegel H. Determination of uric acid and hematin in a single sample of excreta from blood-fed insects. Experientia 1980, 36:1428.
12. Charlwood J.D. Biological variation in Anopheles darlingi root. Mem. Inst. Oswaldo Cruz 1996, 91:391-398.
13. Charlwood J.D., Pinto J., Sousa C.A., Ferreira C., Petrarca V., Rosario Vdo E. 'A mate or a meal' - pre-gravid behaviour of female Anopheles gambiae from the islands of Sao Tome and Principe, West Africa. Malar. J. 2003, 2:9.
14. Chege G.M., Beier J.C. Effect of Plasmodium falciparum on the survival of naturally infected afrotropical Anopheles (Diptera: Culicidae). J. Med. Entomol. 1990, 27:454-458.
15. Churcher T.S., Blagborough A.M., Delves M., Ramakrishnan C., Kapulu M.C., Williams A.R., Biswas S., Da D.F., Cohuet A., Sinden R.E. Measuring the blockade of malaria transmission - an analysis of the standard membrane feeding assay. Int. J. Parasitol. 2012, 42:1037-1044.
16. Cirimotich C.M., Clayton A.M., Dimopoulos G. Low- and high-tech approaches to control Plasmodium parasite transmission by anopheles mosquitoes. J. Trop. Med. 2011, 2011:891342.
17. Cirimotich C.M., Dong Y., Clayton A.M., Sandiford S.L., Souza-Neto J.A., Mulenga M., Dimopoulos G. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 2011, 332:855-858.
18. Coetzee M., Hunt R.H., Wilkerson R., della Torre A., Coulibaly M., Besansky N. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 2013, 3619.
19. Cohuet A., Osta M.A., Morlais I., Awono-Ambene P.H., Michel K., Simard F., Christophides G.K., Fontenille D., Kafatos F.C. Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep. 2006, 7:1285-1289.
20. Cohuet A., Krishnakumar S., Simard F., Morlais I., Koutsos A., Fontenille D., Mindrinos M., Kafatos F.C. SNP discovery and molecular evolution in Anopheles gambiae, with special emphasis on innate immune system. BMC Genomics 2008, 9:227.
21. Costantini C., Li S.G., Della Torre A., Sagnon N., Coluzzi M., Taylor C.E. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a west African Sudan savanna village. Med. Vet. Entomol. 1996, 10:203-219.
22. Crawford J.E., Bischoff E., Garnier T., Gneme A., Eiglmeier K., Holm I., Riehle M.M., Guelbeogo W.M., Sagnon N., Lazzaro B.P., Vernick K.D. Evidence for population-specific positive selection on immune genes of Anopheles gambiae. G3 (Bethesda) 2012, 2:1505-1519.
23. Dao A., Kassogue Y., Adamou A., Diallo M., Yaro A.S., Traore S.F., Lehmann T. Reproduction-longevity trade-off in Anopheles gambiae (Diptera: Culicidae). J. Med. Entomol. 2010, 47:769-777.
24. Dawes E.J., Zhuang S., Sinden R.E., Basanez M.G. The temporal dynamics of Plasmodium density through the sporogonic cycle within Anopheles mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 2009, 103:1197-1198.
25. Dieter K.L., Huestis D.L., Lehmann T. The effects of oviposition-site deprivation on Anopheles gambiae reproduction. Parasit Vectors 2012, 5:235.
26. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006, 2:513-525.
27. Dong Y., Das S., Cirimotich C., Souza-Neto J.A., McLean K.J., Dimopoulos G. Engineered anopheles immunity to Plasmodium infection. PLoS Pathog. 2011, 7:e1002458.
28. Drakeley C., Schellenberg D., Kihonda J., Sousa C.A., Arez A.P., Lopes D., Lines J., Mshinda H., Lengeler C., Armstrong Schellenberg J., Tanner M., Alonso P. An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop. Med. Int. Health 2003, 8:767-774.
29. Emami S.N., Ranford-Cartwright L.C., Ferguson H.M. The impact of low erythrocyte density in human blood on the fitness and energetic reserves of the African malaria vector Anopheles gambiae. Malar. J. 2013, 12:45.
30. Fanello C., Santolamazza F., della Torre A. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med. Vet. Entomol. 2002, 16:461-464.
31. Ferguson H.M., Read A.F. Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proc. Biol. Sci. 2002, 269:1217-1224.
32. Ferguson H.M., Read A.F. Why is the effect of malaria parasites on mosquito survival still unresolved?. Trends Parasitol. 2002, 18:256-261.
33. Harris C., Lambrechts L., Rousset F., Abate L., Nsango S.E., Fontenille D., Morlais I., Cohuet A. Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog. 2010, 6:e1001112.
34. Harris C., Morlais I., Churcher T.S., Awono-Ambene P., Gouagna L.C., Dabire R.K., Fontenille D., Cohuet A. Plasmodium falciparum produce lower infection intensities in local versus foreign Anopheles gambiae populations. PLoS One 2012, 7:e30849.
35. Hogg J.C., Hurd H. The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s. l. in north east Tanzania. Parasitology 1997, 114:325-331.
36. Isaacs A.T., Li F., Jasinskiene N., Chen X., Nirmala X., Marinotti O., Vinetz J.M., James A.A. Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi. PLoS Pathog. 2011, 7:e1002017.
37. Koella, J.C., 2003. On the evolutionary ecology of mosquito immunity and the use of transgenic mosquitoes for malaria control. In: Takken, W., Scott, T.W. (Eds.), Ecological Aspects for Application of Genetically Modified Mosquitoes, Springer.
38. Koella J.C., Zaghloul L. Using evolutionary costs to enhance the efficacy of malaria control via genetically manipulated mosquitoes. Parasitology 2008, 135:1489-1496.
39. Lalubin F., Deledevant A., Glaizot O., Christe P. Natural malaria infection reduces starvation resistance of nutritionally stressed mosquitoes. J. Anim. Ecol. 2014, 10.1111/1365-2656.12190.
40. Lambrechts L., Halbert J., Durand P., Gouagna L.C., Koella J.C. Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar. J. 2005, 4:3.
41. Lambrechts L., Chavatte J.M., Snounou G., Koella J.C. Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proc. Biol. Sci. 2006, 273:1501-1506.
42. Lefevre T., Vantaux A., Dabire K.R., Mouline K., Cohuet A. Non-genetic determinants of mosquito competence for malaria parasites. PLoS Pathog. 2013, 9:e1003365.
43. Lim J., Gowda D.C., Krishnegowda G., Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infect. Immun. 2005, 73:2778-2789.
44. Manda H., Gouagna L.C., Foster W.A., Jackson R.R., Beier J.C., Githure J.I., Hassanali A. Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malar. J. 2007, 6:113.
45. Manda H., Gouagna L.C., Nyandat E., Kabiru E.W., Jackson R.R., Foster W.A., Githure J.I., Beier J.C., Hassanali A. Discriminative feeding behaviour of Anopheles gambiae s.s. on endemic plants in western Kenya. Med. Vet. Entomol. 2007, 21:103-111.
46. Mendes A.M., Schlegelmilch T., Cohuet A., Awono-Ambene P., De Iorio M., Fontenille D., Morlais I., Christophides G.K., Kafatos F.C., Vlachou D. Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa. PLoS Pathog. 2008, 4:e1000069.
47. Mendes A.M., Awono-Ambene P.H., Nsango S.E., Cohuet A., Fontenille D., Kafatos F.C., Christophides G.K., Morlais I., Vlachou D. Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum. Infect. Immun. 2011, 79:4708-4715.
48. Mitri C., Vernick K.D. Anopheles gambiae pathogen susceptibility: the intersection of genetics, immunity and ecology. Curr. Opin. Microbiol. 2012, 15:285-291.
49. Morassin B., Fabre R., Berry A., Magnaval J.F. One year's experience with the polymerase chain reaction as a routine method for the diagnosis of imported malaria. Am. J. Trop. Med. Hyg. 2002, 66:503-508.
50. Moret Y., Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science 2000, 290:1166-1168.
51. Morlais I., Poncon N., Simard F., Cohuet A., Fontenille D. Intraspecific nucleotide variation in Anopheles gambiae: new insights into the biology of malaria vectors. Am. J. Trop. Med. Hyg. 2004, 71:795-802.
52. Mouline K., Mamai W., Agnew P., Tchonfienet M., Brengues C., Dabire R., Robert V., Simard F. Physiology and development of the M and S molecular forms of Anopheles gambiae in Burkina Faso (West Africa). Med. Vet. Entomol. 2012, 26:447-454.
53. Muller G.C., Beier J.C., Traore S.F., Toure M.B., Traore M.M., Bah S., Doumbia S., Schlein Y. Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar. J. 2010, 9:262.
54. Niare O., Markianos K., Volz J., Oduol F., Toure A., Bagayoko M., Sangare D., Traore S.F., Wang R., Blass C., Dolo G., Bouare M., Kafatos F.C., Kruglyak L., Toure Y.T., Vernick K.D. Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science 2002, 298:213-216.
55. Nyasembe V.O., Teal P.E., Sawa P., Tumlinson J.H., Borgemeister C., Torto B. Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake. Curr. Biol. 2014, 24:217-221.
56. Obbard D.J., Callister D.M., Jiggins F.M., Soares D.C., Yan G., Little T.J. The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae. BMC Evol. Biol. 2008, 8:274.
57. Okech B.A., Gouagna L.C., Kabiru E.W., Beier J.C., Yan G., Githure J.I. Influence of age and previous diet of Anopheles gambiae on the infectivity of natural Plasmodium falciparum gametocytes from human volunteers. J. Insect Sci. 2004, 4:33.
58. Okech B.A., Gouagna L.C., Kabiru E.W., Walczak E., Beier J.C., Yan G., Githure J.I. Resistance of early midgut stages of natural Plasmodium falciparum parasites to high temperatures in experimentally infected Anopheles gambiae (Diptera: Culicidae). J. Parasitol. 2004, 90:764-768.
59. Pakpour N., Corby-Harris V., Green G.P., Smithers H.M., Cheung K.W., Riehle M.A., Luckhart S. Ingested human insulin inhibits the mosquito NF-kappaB-dependent immune response to Plasmodium falciparum. Infect. Immun. 2012, 80:2141-2149.
60. Riehle M.M., Markianos K., Niare O., Xu J., Li J., Toure A.M., Podiougou B., Oduol F., Diawara S., Diallo M., Coulibaly B., Ouatara A., Kruglyak L., Traore S.F., Vernick K.D. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 2006, 312:577-579.
61. Robert V., Verhave J.P., Carnevale P. Plasmodium falciparum infection does not increase the precocious mortality rate of Anopheles gambiae. Trans. R. Soc. Trop. Med. Hyg. 1990, 84:346-347.
62. Robert V., Le Goff G., Essong J., Tchuinkam T., Faas B., Verhave J.P. Detection of falciparum malarial forms in naturally infected anophelines in Cameroon using a fluorescent anti-25-kD monoclonal antibody. Am. J. Trop. Med. Hyg. 1995, 52:366-369.
63. Rossignol P.A., Ribeiro J.M., Spielman A. Increased intradermal probing time in sporozoite-infected mosquitoes. Am. J. Trop. Med. Hyg. 1984, 33:17-20.
64. Sangare I., Michalakis Y., Yameogo B., Dabire R., Morlais I., Cohuet A. Studying fitness cost of Plasmodium falciparum infection in malaria vectors: validation of an appropriate negative control. Malar. J. 2013, 12:2.
65. Schmid-Hempel P. Variation in immune defence as a question of evolutionary ecology. Proc. Biol. Sci. 2003, 270:357-366.
66. Schwartz A., Koella J.C. The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. J. Evol. Biol. 2004, 17:834-840.
67. Sheldon B.C., Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Evol. Ecol. 1996, 11:317-321.
68. Sinkins S.P., Gould F. Gene drive systems for insect disease vectors. Nat. Rev. Genet. 2006, 7:427-435.
69. Smith D.L., McKenzie F.E. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar. J. 2004, 3:13.
70. Tahar R., Boudin C., Thiery I., Bourgouin C. Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J. 2002, 21:6673-6680.
71. Takken W., Klowden M.J., Chambers G.M. Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): the disadvantage of being small. J. Med. Entomol. 1998, 35:639-645.
72. Tripet F. Ecological immunology of mosquito-malaria interactions: of non-natural versus natural model systems and their inferences. Parasitology 2009, 136:1935-1942.
73. Tripet F., Aboagye-Antwi F., Hurd H. Ecological immunology of mosquito-malaria interactions. Trends Parasitol. 2008, 24.
74. Vaughan J.A., Noden B.H., Beier J.C. Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. J. Parasitol. 1992, 78:716-724.
75. Vezilier J., Nicot A., Gandon S., Rivero A. Plasmodium infection decreases fecundity and increases survival of mosquitoes. Proc. Biol. Sci. 2012, 279:4033-4041.
76. Wekesa J.W., Copeland R.S., Mwangi R.W. Effect of Plasmodium falciparum on blood feeding behavior of naturally infected Anopheles mosquitoes in western Kenya. Am. J. Trop. Med. Hyg. 1992, 47:484-488.
77. Zele F., Nicot A., Duron O., Rivero A. Infection with Wolbachia protects mosquitoes against Plasmodium-induced mortality in a natural system. J. Evol. Biol. 2012, 25:1243-1252.