Existing Infection Facilitates Establishment and Density of Malaria Parasites in Their Mosquito Vector

PLoS Pathogens

Volumn 11, Issue 7, 2015, Pages

  Pollitt, Laura C ^a,b   Bram, Joshua T ^b   Blanford, Simon ^b   Jones, Matthew J ^b   Read, Andrew F ^b,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL MODEL; ANOPHELES STEPHENSI; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DISEASE TRANSMISSION; FEMALE; FLOW CYTOMETRY; MALARIA; MIXED INFECTION; MOSQUITO; MOUSE; NONHUMAN; PARASITE VECTOR; PARASITE VIRULENCE; PLASMODIUM; PLASMODIUM CHABAUDI; POLYMERASE CHAIN REACTION; SECONDARY INFECTION; SURVIVAL RATE; ANIMAL; EVOLUTION; FEEDING BEHAVIOR; HOST PATHOGEN INTERACTION; PARASITOLOGY; PHYSIOLOGY; TRANSMISSION;

VERTEBRATA;

ANIMALS; BIOLOGICAL EVOLUTION; CULICIDAE; FEEDING BEHAVIOR; HOST-PATHOGEN INTERACTIONS; MALARIA;

EID: 84938771571     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005003     Document Type: Article

References (60)

1. Balmer O, Tanner M, Prevalence and implications of multiple-strain infections. Lancet Infect Dis. 2011;11: 868–878. doi: 10.1016/S1473-3099(11)70241-9 22035615
2. Raberg L, de Roode JC, Bell AS, Stamou P, Gray D, et al. The role of immune-mediated apparent competition in genetically diverse malaria infections. Am Nat. 2006;168: 41–53. 16874614
3. Read AF, The ecology of genetically diverse infections. Science. 2001;292: 1099–1102. 11352063
4. Bossert WH, McKenzie FE, Mixed-species Plasmodium infections of Anopheles (Diptera: Culicidae). J Med Entomol. 1997;34: 417. 9220675
5. Read AF, Day T, Huijben S, The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. Proc Natl Acad Sci USA. 2011;108: 10871–10877. doi: 10.1073/pnas.1100299108 21690376
6. Pollitt LC, Huijben S, Sim DG, Salathé RM, Jones MJ, et al. Rapid response to selection, competitive release and increased transmission potential of artesunate-selected Plasmodium chabaudi malaria parasites. PLoS Pathog. 2014;10: e1004019. doi: 10.1371/journal.ppat.1004019 24763470
7. Alizon S, de Roode JC, Michalakis Y, Multiple infections and the evolution of virulence. Ecol Lett. 2013;16: 556–567. doi: 10.1111/ele.12076 23347009
8. de Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, et al. Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA. 2005;102: 7624–7628. 15894623
9. Pollitt LC, Mideo N, Drew DR, Schneider P, Colegrave N, et al. Competition and the evolution of reproductive restraint in malaria parasites. Am Nat. 2011;177: 358–367. doi: 10.1086/658175 21460544
10. Daubersies P, Sallenave-Sales S, Magne S, Trape JF, Contamin H, et al. Rapid turnover of Plasmodium falciparum populations in asymptomatic individuals living in a high transmission area. Am J Trop Med Hyg. 1996;54: 18–26. 8651363
11. Mercereau-Puijalon O, Revisiting host/parasite interactions: molecular analysis of parasites collected during longitudinal and cross-sectional surveys in humans. Parasite Immunol. 1996;18: 173–180. 9223172
12. Smith T, Felger I, Tanner M, Beck HP, Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg. 1999;93: 59–64. 10450428
13. Bruce MC, Donnelly CA, Alpers MP, Galinski MR, Barnwell JW, et al. Cross-species interactions between malaria parasites in humans. Science. 2000;287: 845–848. 10657296
14. Hastings IM, Malaria control and the evolution of drug resistance: an intriguing link. Trends Parasitol. 2003;19: 70–73. 12586474
15. Talisuna AO, Erhart A, Samarasinghe S, Van Overmeir C, Speybroeck N, et al. Malaria transmission intensity and the rate of spread of chloroquine resistant Plasmodium falciparum: Why have theoretical models generated conflicting results? Infect Genet Evol. 2006;6: 241–248. 16112915
16. Bousema JT, Drakeley CJ, Mens PF, Arens T, Houben R, et al. Increased Plasmodium falciparum gametocyte production in mixed infections with P. malariae. Am J Trop Med Hyg. 2008;78: 442–448. 18337341
17. Baliraine FN, Afrane YA, Amenya DA, Bonizzoni M, Vardo-Zalik AM, et al. A cohort study of Plasmodium falciparum infection dynamics in Western Kenya Highlands. BMC Infect Dis. 2010;10: 283. doi: 10.1186/1471-2334-10-283 20868504
18. Paaijmans KP, Blanford S, Chan BHK, Thomas MB, Warmer temperatures reduce the vectorial capacity of malaria mosquitoes. Biol Lett. 2012;8: 465–468. doi: 10.1098/rsbl.2011.1075 22188673
19. Sinden RE, Dawes EJ, Alavi Y, Waldock J, Finney O, et al. Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLoS Pathog. 2007;3: e195. doi: 10.1371/journal.ppat.0030195 18166078
20. Pollitt LC, Churcher TS, Dawes EJ, Khan SM, Sajid M, et al. Costs of crowding for the transmission of malaria parasites. Evol Appl. 2013;6: 617–629. doi: 10.1111/eva.12048 23789029
21. Churcher TS, Dawes EJ, Sinden RE, Christophides GK, Koella JC, et al. Population biology of malaria within the mosquito: density-dependent processes and potential implications for transmission-blocking interventions. Malar J. 2010;9: 311. doi: 10.1186/1475-2875-9-311 21050427
22. Dawes EJ, Churcher TS, Zhuang S, Sinden RE, Basáñez M-G, Anopheles mortality is both age- and Plasmodium-density dependent: implications for malaria transmission. Malar J. 2009;8: 228. doi: 10.1186/1475-2875-8-228 19822012
23. Taylor LH, Infection rates in, and the number of Plasmodium falciparum genotypes carried by Anopheles mosquitoes in Tanzania. Annals of Tropical Medicine and Parasitology. 1999;93: 659–662. 10707111
24. Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, et al. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology. 1994;109: 413–421. 7800409
25. Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, et al. Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc Natl Acad Sci USA. 2010;107: 20138–20143. doi: 10.1073/pnas.1007068107 21041629
26. Bell AS, Huijben S, Paaijmans KP, Sim DG, Chan BHK, et al. Enhanced transmission of drug-resistant parasites to mosquitoes following drug treatment in rodent malaria. PLoS ONE. 2012;7: e37172. doi: 10.1371/journal.pone.0037172 22701563
27. Beier JC, Malaria parasite development in mosquitoes. Annu Rev Entomol. 1998;43: 519–543. 9444756
28. Norris LC, Fornadel CM, Hung WC, Pineda FJ, Norris DE, Frequency of multiple blood meals taken in a single gonotrophic cycle by Anopheles arabiensis mosquitoes in Macha, Zambia. Am J Trop Med Hyg. 2010;83: 33–37. doi: 10.4269/ajtmh.2010.09-0296 20595474
29. Scott TW, Githeko AK, Fleisher A, Harrington LC, Yan G, DNA profiling of human blood in anophelines from lowland and highland sites in western Kenya. Am J Trop Med Hyg. 2006;75: 231–237. 16896124
30. Boyd MF, Boyd MF, Epidemiology: Factors related to the definitive host. In: Malariology. A comprehensive survey of all aspects of this group of diseases from a global standpoint. Volume 1. Philadelphia: W. B. Saunders Company, Vol. 1. 1949. pp. 609–697.
31. Daniels CW, Summary of researches on the propagation of malaria in British Central Africa. British medical journal. 1901;1: 193.
32. Garnham PCC, Malaria parasites and other haemosporidia. 1st ed. Oxford: blackwell scientific publications; 1966.
33. Huff CG, Individual Immunity and Susceptibility of Culex pipiens to various Species of Bird Malaria as studied by means of double infectious Feedings. American Journal of Hygiene. 1930;12: 424–441.
34. Kuehn A, Pradel G, The coming-out of malaria gametocytes. J Biomed Biotechnol. 2010;2010: 976827. doi: 10.1155/2010/976827 20111746
35. Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, et al. A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg. 2000;62: 535–544. 11289661
36. Cator LJ, George J, Blanford S, Murdock CC, Baker TC, et al. “Manipulation” without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites. Proc R Soc Lond B Biol Sci. 2013;280: 20130711.
37. Paaijmans KP, Cator LJ, Thomas MB, Temperature-dependent pre-bloodmeal period and temperature-driven asynchrony between parasite development and mosquito biting rate reduce malaria transmission intensity. PLoS ONE. 2013;8: e55777. doi: 10.1371/journal.pone.0055777 23383280
38. Ponnudurai T, Lensen AH, van Gemert GJ, Bolmer M, van Belkum A, et al. Large-scale production of Plasmodium vivax sporozoites. Parasitol. 1990;101: 317–320.
39. Hogg JC, Carwardine S, Hurd H, The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Parasitology Research. 1997;83: 374–379. 9134561
40. Aboagye-Antwi F, Guindo A, Traoré AS, Hurd H, Coulibaly M, et al. Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes. Malar J. 2010;9: 243. doi: 10.1186/1475-2875-9-243 20796288
41. Bell AS, de Roode JC, Sim D, Read AF, Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution. 2006;60: 1358–1371. 16929653
42. Reece SE, Drew DR, Gardner A, Sex ratio adjustment and kin discrimination in malaria parasites. Nature. 2008;453: 609–614. doi: 10.1038/nature06954 18509435
43. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C, Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science. 2010;329: 1353–1355. doi: 10.1126/science.1190689 20829487
44. Pringle G, A quantitative study of naturally-acquired malaria infections in Anopheles Gambiae and Anopheles funestus in a highly malarious area of East Africa. Trans R Soc Trop Med Hyg. 1996;60: 626–632.
45. Annan Z, Durand P, Ayala FJ, Arnathau C, Awono-Ambene P, et al. Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proc Natl Acad Sci USA. 2007;104: 7987–7992. 17470800
46. Cator LJ, Lynch PA, Thomas MB, Read AF, Alterations in mosquito behaviour by malaria parasites: potential impact on force of infection. Malar J. 2014;13: 164. doi: 10.1186/1475-2875-13-164 24885783
47. Read AF, Lynch PA, Thomas MB, (2009) How to make evolution-proof insecticides for malaria control. PLos Biol 7:e1000058. doi: 10.1371/journal.pbio.1000058 19355786
48. Ferguson HM, Read AF, Mosquito appetite for blood is stimulated by Plasmodium chabaudi infections in themselves and their vertebrate hosts. Malar J. 2004;3: 12. 15151700
49. De Moraes CM, Stanczyk NM, Betz HS, Pulido H, Sim DG, et al. Malaria-induced changes in host odors enhance mosquito attraction. Proc Natl Acad Sci USA. 2014;111: 11079–11084. doi: 10.1073/pnas.1405617111 24982164
50. Mayagaya VS, Michel K, Benedict MQ, Killeen GF, Wirtz RA, et al. Non-destructive determination of age and species of Anopheles gambiae s.l. using near-infrared spectroscopy. Am J Trop Med Hyg. 2009;81: 622–630. doi: 10.4269/ajtmh.2009.09-0192 19815877
51. Wiesch zur PA, Kouyos R, Engelstädter J, Regoes RR, Bonhoeffer S, Population biological principles of drug-resistance evolution in infectious diseases. Lancet Infect Dis. 2011;11: 236–247. doi: 10.1016/S1473-3099(10)70264-4 21371657
52. Harrington WE, Mutabingwa TK, Muehlenbachs A, Sorensen B, Bolla MC, et al. Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proc Natl Acad Sci USA. 2009;106: 9027–9032. doi: 10.1073/pnas.0901415106 19451638
53. Färnert A, Plasmodium falciparum population dynamics: only snapshots in time? Trends Parasitol. 2008;24: 340–344. doi: 10.1016/j.pt.2008.04.008 18617441
54. Carter R, Studies on enzyme variation in the murine malaria parasites Plasmodium berghei, P. yoelii, P. vinckei and P. chabaudi by starch gel electrophoresis. Parasitology. 1978;76: 241–267. 351525
55. Jacobs RL, Role of P-Aminobenzoic acid in Plasmodium berghei infection in the mouse. Exp Parasitol. 1964;15: 213–225. 14191322
56. Ferguson HM, Mackinnon MJ, Chan BH, Read AF, Mosquito mortality and the evolution of malaria virulence. Evolution. 2003;57: 2792–2804. 14761058
57. Bell AS, Huijben S, Paaijmans KP, Sim DG, Chan BHK, et al. Enhanced transmission of drug-resistant parasites to mosquitoes following drug treatment in rodent malaria. PLoS ONE. 2012;7: e37172. doi: 10.1371/journal.pone.0037172 22701563
58. Boncristiani H, Li J, Evans JD, Pettis J, Chen Y, Scientific note on PCR inhibitors in the compound eyes of honey bees, Apis mellifera. Apidologie. 2011;42: 457–460.
59. Kreader CA, Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl Environ Microbiol. 1996;62: 1102–1106. 8975603
60. Pollitt LC, Bram JT, Blanford S, Jones MJ, Read AF, (2015) Data from: Existing infection facilitates establishment and density of malaria parasites in their mosquito vector. Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.8nr13