Evolution of Plastic Transmission Strategies in Avian Malaria

PLoS Pathogens

Volumn 10, Issue 9, 2014, Pages

  Cornet, Stéphane ^a,b   Nicot, Antoine ^a,b   Rivero, Ana ^b   Gandon, Sylvain ^a  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVIAN MALARIA; BIRD; CONTROLLED STUDY; CULEX PIPIENS; DISEASE CARRIER; DISEASE TRANSMISSION; EXPOSURE; FEMALE; NONHUMAN; PARASITEMIA; PLASMODIUM; PLASMODIUM RELICTUM; PLASTICITY; PREVALENCE; SEASONAL VARIATION; THEORY; ANIMAL; CULEX; EVOLUTION; HOST PARASITE INTERACTION; MOSQUITO; PARASITOLOGY; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; TRANSMISSION;

AVES;

ANIMALS; BIOLOGICAL EVOLUTION; BIRDS; CULEX; CULICIDAE; FEMALE; HOST-PARASITE INTERACTIONS; INSECT VECTORS; MALARIA, AVIAN; PHYLOGENY; PLASMODIUM;

EID: 84907587723     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004308     Document Type: Article

References (100)

1. Meyers LA, Bull JJ, (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17: 551–557.
2. Massey RC, Buckling A, Peacock SJ, (2001) Phenotypic switching of antibiotic resistance circumvents permanent costs in Staphylococcus aureus. Curr Biol 11: 1810–1814.
3. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S, (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622–1625.
4. Stewart FM, Levin BR, (1984) The population biology of bacterial viruses: why be temperate. Theor Pop Biol 26: 93–117.
5. Stumpf MPH, Laidlaw Z, Jansen VAA, (2002) Herpes viruses hedge their bets. Proc Natl Acad Sci USA 99: 15234–15237.
6. Trape JF, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, et al. (1992) Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg 47: 181–189.
7. Rogers DJ, Randolph SE, Snow RW, Hay SI, (2002) Satellite imagery in the study and forecast of malaria. Nature 415: 710–715.
8. Mbogo CM, Mwangangi JM, Nzovu J, Gu W, Yan G, et al. (2003) Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg 68: 734–742.
9. Oesterholt MJAM, Bousema JT, Mwerinde OK, Harris C, Lushino P, et al. (2006) Spatial and temporal variation in malaria transmission in a low endemicity area in northern Tanzania. Malaria J 5: 98.
10. Paul REL, Diallo M, Brey PT, (2004) Mosquitoes and transmission of malaria parasites - not just vectors. Malaria J 3: e39.
11. Ponçon N, Toty C, L'AMBERT G, Le Goff G, Brengues C, et al. (2007) Population dynamics of pest mosquitoes and potential malaria and West Nile virus vectors in relation to climatic factors and human activities in the Camargue, France. Med Vet Entomol 21: 350–357.
12. White NJ, (2011) Determinants of relapse periodicity in Plasmodium vivax malaria. Malaria J 10: 297.
13. McLean SA, Person CD, Phillips RS, (1982) Plasmodium chabaudi: relationship between the occurence of recrudescenct parasitaemias in mice and the effective levels of acquired immunity. Exp Parasitol 54: 213–221.
14. Huff CG, Bloom W, (1935) A malarial parasite infecting all blood and blood-forming cells of birds. J Infect Dis 57: 315–336.
15. James SP, Tate P, (1937) New knowledge of the life-cycle of malaria parasites. Nature 139: 545.
16. Shortt HE, Garnham PCC, Covell G, Shute PG, (1948) Pre-erythrocytic stage of human malaria, Plasmodium vivax. Brit Med J 1: 547.
17. Cogswell FB, (1992) The hypnozoite and relapse in primate malaria. Clin Microbiol Rev 5: 26–35.
18. Thompson PE, Huff CG, (1944) A saurian malarial parasite, Plasmodium mexicanum, N. Sp., with both elongatum and gallinaceum-types of exoerythrocytic stages. J Infect Dis 74: 48–67.
19. Telford SR, Jr (1989) Discovery of the pre-erythrocytic stages of a saurian malaria parasite, hypnozoites, and a possible mechanism for the maintenance of chronic infections throughout the life of the host. Int J Parasitol 19: 597–616.
20. Thayer WLotmf, p. 326. (1897) Lectures on the malarial fevers. New York: D. Appleton & Co.
21. Coatney GR, (1976) Relapse in malaria: an enigma. J Parasitol 62: 2–9.
22. Battle KE, Karhunen MS, Bhatt S, Gething PW, Howes RE, et al. (2014) Geographical variation in Plasmodium vivax relapse. Malaria J 13: 144.
23. Allan RA, Mahrt JL, (1989) Influence of transmission period on primary and relapse patterns of infection of Leucocytozoon spp. and Haemoproteus mansoni. Am Midl Nat 121: 341–349.
24. Pigliucci M, (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20: 481–486.
25. Scheiner SM, (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24: 35–68.
26. Reece SE, Ramiro RS, Nussey DH, (2009) Plastic parasites: sophisticated strategies for survival and reproduction? Evol Appl 2: 11–23.
27. Babayan SA, Read AF, Lawrence RA, Bain O, Allen JE, (2010) Filarial parasites develop faster and reproduce earlier in response to host immune effectors that determine filarial life expectancy. PLoS Biol 8: e1000525.
28. Leggett HC, Benmayor R, Hodgson DJ, Buckling A, (2013) Experimental Evolution of Adaptive Phenotypic Plasticity in a Parasite. Curr Biol 23: 139–142.
29. Reece SE, Ali E, Schneider P, Babiker HA, (2010) Stress, drugs and the evolution of reproductive restraint in malaria parasites. Proc R Soc B Biol Sci 277: 3123–3129.
30. Pollitt LC, Mideo N, Drew DR, Schneider P, Colegrave N, et al. (2011) Competition and the evolution of reproductive restraint in malaria parasites. Am Nat 177: 358–367.
31. Hulden L, Hulden L, (2011) Activation of the hypnozoite: a part of Plasmodium vivax life cycle and survival. Malaria J 10: 90.
32. Manwell RD, (1929) Relapse in bird malaria. Am J Epidemiol 9: 308–345.
33. Appelgate JE, (1970) Population changes in latent avian malaria infections associated with season and corticosterone treatment. J Parasitol 56: 439–443.
34. Appelgate JE, Beaudoin RL, (1970) Mechanisms of spring relapse in avian malaria: effects of gonodropin and corticosterone. J Wildlife Dis 6: 443–447.
35. Pearson RD, (2002) Is prolactin responsible for avian, saurian, and mammalian relapse and periodicity of fever in malarial infections? Can J Zool 80: 1313–1315.
36. Valkiunas G, Bairlein F, Iezhova TA, Dolnik OV, (2004) Factors affecting the relapse of Haemoproteus belopolskyi infections and the parasitaemia of Trypanosoma spp. in a naturally infected European songbird, the blackcap, Sylvia atricapilla. Parasitol Res 93: 218–222.
37. Hulden L, Hulden L, Heliovaara K, (2008) Natural relapses in vivax malaria induced by Anopheles mosquitoes. Malaria J 7: 64.
38. Lawaly R, Konate L, Marrama L, Dia I, Diallo D, et al. (2012) Impact of mosquito bites on asexual parasite density and gametocyte prevalence in asymptomatic chronic Plasmodium falciparum infections and correlation with IgE and IgG titers. Infect Immun 80: 2240–2246.
39. Billingsley PF, Snook LS, Johnston VJ, (2005) Malaria parasite growth is stimulated by mosquito probing. Biol Lett 1: 185–189.
40. Shutler D, Reece SE, Mullie A, Billingsley PF, Read AF, (2005) Rodent malaria parasites Plasmodium chabaudi and P. vinckei do not increase their rates of gametocytogenesis in response to mosquito probing. Proc R Soc B Biol Sci 272: 2397–2402.
41. Killick-Kendrick R (1978) Taxonomy, zoology and evolution. In: Killick-Kendrick R, Peters W, editors. Rodent Malaria. London: Academic Press. pp. 1–52.
42. Landau I, Chabaud A, (1994) Plasmodium species infecting Thamnomys rutilans: a zoological study. Adv Parasitol 33: 50–90.
43. Roca-Feltrer A, Schellenberg JR, Smith L, Carneiro I, (2009) A simple method for defining malaria seasonality. Malaria J 8: 276.
44. Valkiūnas G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, FL., USA: CRC Press.
45. Frank SA, (1996) Models of parasite virulence. Q Rev Biol 71: 37–78.
46. Alizon SA, Hurford A, Mideo N, van Baalen M, (2009) Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol 22: 245–259.
47. Beldade P, Mateus ARA, Keller RA, (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20: 1347–1363.
48. Duneau D, Ebert D, (2012) Host sexual dimorphism and parasite adaptation. PLoS Biol 10: e1001271.
49. Mideo N, Reece SE, (2012) Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiol 7: 17–24.
50. Van Den Berg F, Bacaër N, Metz JAJ, Lannou C, Van Den Bosch F, (2011) Periodic host absence can select for higher or lower parasite transmission rates. Evol Ecol 25: 121–137.
51. Donnelly R, Best A, White A, Boots M, (2013) Seasonality selects for more acutely virulent parasites when virulence is density dependent. Proceedings of the Royal Society B: Biological Sciences, 280(1751). Proc R Soc B Biol Sci 280: 20122464.
52. Koelle K, Pascual M, Yunus M, (2005) Pathogen adaptation to seasonal forcing and climate change. Proc R Soc B Biol Sci 272: 971–977.
53. Kamo M, Sasaki A, (2005) Evolution toward multi-year periodicity in epidemics. Ecol Lett 8: 378–385.
54. Cohen D, (1967) Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. J Theor Biol 16: 1–14.
55. Gavrilets S, Scheiner SM, (1993) The genetics of phenotypic plasticity. 5. Evolution of reaction norm shape. J Evol Biol 6: 31–48.
56. Lande R, (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22: 1435–1446.
57. Cellier-Holzem E, Esparza-Salas R, Garnier S, Sorci G, (2010) Effect of repeated exposure to Plasmodium relictum (lineage SGS1) on infection dynamics in domestic canaries. Int J Parasitol 40: 1447–1453.
58. Reece SE, Drew DR, Gardner A, (2008) Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453: 609–614.
59. Babiker HA, Schneider P, Reece SE, (2008) Gametocytes: insights gained during a decade of molecular monitoring. Trends Parasitol 24: 525–530.
60. Abdel-Wahab A, Abdel-Muhsin AMA, Ali E, Suleiman S, Ahmed S, et al. (2002) Dynamics of gametocytes among Plasmodium falciparum clones in natural infections in an area of highly seasonal transmission. J Infect Dis 185: 1838–1842.
61. Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, et al. (2004) Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol 137: 35–41.
62. Schneider P, Bousema JT, Gouagna LC, Otieno S, Van de Vegte-Bolmer M, et al. (2007) Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg 76: 470–474.
63. Okech BA, Gouagna LC, Kabiru EW, Beier JC, Yan GY, et al. (2004) Influence of age and previous diet of Anopheles gambiae on the infectivity of natural Plasmodium falciparum gametocytes from human volunteers. J Insect Sci 4: 33.
64. Terzian LA, Stahler N, Irreverre F, (1956) The effects of aging, and the modifications of these effects, on the immunity of mosquitoes to malarial infection. J Immunol 76: 308–313.
65. Fontaine A, Diouf I, Bakkali N, Misse D, Pages F, et al. (2011) Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasites Vectors 4: 187.
66. Titus RG, Ribeiro JM, (1988) Salivary gland lysates from the sand fly Lutzomyialongipalpis enhance Leishmania infectivity. Science 239: 1306–1308.
67. Cameron A, Reece SE, Drew DR, Haydon DT, Yates AJ, (2013) Plasticity in transmission strategies of the malaria parasite, Plasmodium chabaudi: environmental and genetic effects. Evol Appl 6: 365–376.
68. Carter LM, Kafsack BFC, Llinas M, Mideo N, Pollitt LC, et al. (2013) Stress and sex in malaria parasites: Why does commitment vary? Evol Med Publ Heath 2013: 135–147.
69. Gautret P, Coquelin F, Chabaud AG, Landau I, (1997) The production of gametocytes by rodent Plasmodium species in mice during phenylhydrazine induced reticulocytosis. Acta Parasitol 42: 65–67.
70. Reece SE, Duncan AB, West SA, Read AF, (2005) Host cell preference and variable transmission strategies in malaria parasites. Proc R Soc B Biol Sci 272: 511–517.
71. Paul REL, Coulson TN, Raibaud A, Brey PT, (2000) Sex determination in malaria parasites. Science 287: 128–131.
72. Drew DR, Reece SE, (2007) Development of reverse-transcription PCR techniques to analyse the density and sex ratio of gametocytes in genetically diverse Plasmodium chabaudi infections. Mol Biochem Parasitol 156: 199–209.
73. Martiniere A, Bak A, Macia JL, Lautredou N, Gargani D, et al. (2013) A virus responds instantly to the presence of the vector on the host and forms transmission morphs. eLife 2: e00183.
74. O'Donnell AJ, Schneider P, McWatters HG, Reece SE, (2011) Fitness costs of disrupting circadian rhythms in malaria parasites. Proc R Soc B Biol Sci 278: 2429–2436.
75. Hawking F, Worms MJ, Gammage K, Goddard PA, (1966) The biological purpose of the blood-cycle of the malaria parasite Plasmodium cynomolgi. Lancet 288: 422–424.
76. Mideo N, Reece SE, Smith AL, Metcalf CJE, (2013) The Cinderella syndrome: why do malaria-infected cells burst at midnight? Trends Parasitol 29: 10–16.
77. Greischar MA, Read AF, Bjørnstad ON, (2014) Synchrony in malaria infections: How intensifying within-host competition can be adaptive. Am Nat 183: E36–E49.
78. Mayxay M, Pukrittayakamee S, Newton PN, White NJ, (2004) Mixed-species malaria infections in humans. Trends Parasitol 20: 233–240.
79. Valkiūnas G, Bensch S, Iezhova TA, Križanauskienė A, Hellgren O, et al. (2006) Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. J Parasitol 92: 418–422.
80. Shanks GD, White NJ, (2013) The activation of vivax malaria hypnozoites by infectious diseases. Lancet Infect Dis 13: 900–906.
81. Chen NH, Auliff A, Rieckmann K, Gatton M, Cheng Q, (2007) Relapses of Plasmodium vivax infection result from clonal hypnozoites activated at predetermined intervals. J Infect Dis 195: 934–941.
82. Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, et al. (2007) Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis 195: 927–933.
83. Bensch S, Hellgren O, Perez-Tris J, (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9: 1353–1358.
84. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, et al. (2012) Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med 9: e1001165.
85. Gilden D, Mahalingam R, Nagel MA, Pugazhenthi S, Cohrs RJ, (2011) Review: the neurobiology of varicella zoster virus infection. Neuropath Appl Neurobiol 37: 441–463.
86. Wilson AC, Mohr I, (2012) A cultured affair: HSV latency and reactivation in neurons. Trends Microbiol 20: 604–611.
87. Cardona PJ, Ruiz-Manzano J, (2004) On the nature of Mycobacterium tuberculosis-latent bacilli. Eur Respir J 24: 1044–1051.
88. Marcello A, (2006) Latency: the hidden HIV-1 challenge. Retrovirology 3: 7.
89. Perng GC, Jones C, (2010) Towards an understanding of the herpes simplex virus type 1 latency-reactivation cycle. Interdisc Persp Infect Dis vol 2010: 262415.
90. Lieberman PM, (2013) Keeping it quiet: chromatin control of gammaherpesvirus latency. Nature Rev Microbiol 11: 863–875.
91. Spina CA, Anderson J, Archin NM, Bosque A, Chan J, et al. (2013) An in-depth comparison of latent HIV-1 reactivation in multiple cell model systems and resting CD4+ T cells from aviremic patients. PLoS Pathog 9: e1003834.
92. Kimura M, Darbro JM, Harrington LC, (2010) Avian malaria parasites share congeneric mosquito vectors. J Parasitol 96: 144–151.
93. Lalubin F, Delédevant A, Glaizot O, Christe P, (2013) Temporal changes in mosquito abundance (Culex pipiens), avian malaria prevalence and lineage composition. Parasites Vectors 6: 307.
94. Vézilier J, Nicot A, Gandon S, Rivero A, (2010) Insecticide resistance and malaria transmission: infection rate and oocyst burden in Culex pipiens mosquitoes infected with Plasmodium relictum. Malaria J 9: 379.
95. Griffiths R, Double MC, Orr K, Dawson RJG, (1998) A DNA test to sex most birds. Mol Ecol 7: 1071–1075.
96. Waldenström J, Bensch S, Hasselquist D, Ostman O, (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90: 191–194.
97. Cornet S, Nicot A, Rivero A, Gandon S, (2013) Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecol Lett 16: 323–329.
98. Huff CG, (1947) Life cycle of malarial parasites. Annual Reviews in Microbiology 1: 43–60.
99. Griffing SM, Kilpatrick AM, Clark L, Marra PP, (2007) Mosquito landing rates on nesting American robins (Turdus migratorius). Vector-Borne Zoo Dis 7: 437–443.
100. Crawley MJ (2007) The R Book. England: John Wiley & Sons, Ltd.