Plasticity in transmission strategies of the malaria parasite, Plasmodium chabaudi: Environmental and genetic effects

Evolutionary Applications

Volumn 6, Issue 2, 2013, Pages 365-376

  Cameron, Angus ^a,b   Reece, Sarah E ^c   Drew, Damien R ^c,d   Haydon, Daniel T ^a   Yates, Andrew J ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d BURNET INSTITUTE   (Australia)

Author keywords

Gametocyte; Gametocytogenesis; Life history trait; Parasite ecology; Phenotypic plasticity; Resource allocation trade off; Transmission strategies

Indexed keywords

EID: 84874092911     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12005     Document Type: Article

References (65)

1. Alizon, S., and M. van Baalen. 2008. Acute or chronic? Within-host models with immune dynamics, infection outcome, and parasite evolution The American Naturalist 172:E244-E256.
2. Babiker, H. A., P. Schneider, and S. E. Reece. 2008. Gametocytes: insights gained during a decade of molecular monitoring. Trends in Parasitology 24:525-530.
3. Bell, A. S., J. C. De Roode, D. Sim, and A. F. Read. 2006. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60:1358-1371.
4. Bousema, T., and C. Drakeley. 2011. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clinical Microbiology Reviews 24:377-410.
5. Buckling, A., and A. F. Read. 2001. The effect of partial host immunity on the transmission of malaria parasites. Proceedings of the Royal Society of London Series B-Biological Sciences 268:2325-2330.
6. Buckling, A. G. J., L. H. Taylor, J. M. R. Carlton, and A. F. Read. 1997. Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proceedings of the Royal Society of London Series B-Biological Sciences 264:553-559.
7. Buckling, A., L. Crooks, and A. Read. 1999a. Plasmodium chabaudi: effect of antimalarial drugs on gametocytogenesis. Experimental Parasitology 93:45-54.
8. Buckling, A., L. C. Ranford-Cartwright, A. Miles, and A. F. Read. 1999b. Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology 118:339-346.
9. Bull, J. J. 1994. Perspective - virulence. Evolution 48:1423-1437.
10. Carter, R., R. W. Gwadz, and I. Green. 1979. Plasmodium gallinaceum - transmission-blocking immunity in chickens. 2. Effect of anti-gamete antibodies in vitro and in vivo and their elaboration during infection. Experimental Parasitology 47:194-208.
11. Clutton-Brock, T. H. 1984. Reproductive effort and terminal investment in iteroparous animals. The American Naturalist 123:212-229.
12. Cohuet, A., C. Harris, V. Robert, and D. Fontenille. 2010. Evolutionary forces on Anopheles: what makes a malaria vector? Trends in Parasitology 26:130-136.
13. Collins, W. E., G. M. Jeffery, and J. M. Roberts. 2004. A retrospective examination of the effect of fever and microgametocyte count on mosquito infection on humans infected with Plasmodium vivax. American Journal of Tropical Medicine and Hygiene 70:638-641.
14. Cotter, S. C., R. J. S. Ward, and R. M. Kilner. 2010. Age-specific reproductive investment in female burying beetles: independent effects of state and risk of death. Functional Ecology 25:652-660.
15. Day, T. 2003. Virulence evolution and the timing of disease life-history events. Trends in Ecology & Evolution 18:113-118.
16. Dixon, M. W. A., J. Thompson, D. L. Gardiner, and K. R. Trenholme. 2008. Sex in Plasmodium: a sign of commitment. Trends in Parasitology 24:168-175.
17. Drakeley, C. J., I. Secka, S. Correa, B. M. Greenwood, and G. A. Targett. 1999. Host haematological factors influencing the transmission of Plasmodium falciparum gametocytes to Anopheles gambiae s.s. mosquitoes. Tropical Medicine & International Health 4:131-138.
18. Drakeley, C., C. Sutherland, J. T. Bousema, R. W. Sauerwein, and G. A. Targett. 2006. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends in Parasitology 22:424-430.
19. Drew, D. R., and S. E. Reece. 2007. Development of reverse-transcription PCR techniques to analyse the density and sex ratio of gametocytes in genetically diverse Plasmodium chabaudi infections. Molecular and Biochemical Parasitology 156:199-209.
20. Evans, K. J., D. S. Hansen, N. van Rooijen, L. A. Buckingham, and L. Schofield. 2006. Severe malarial anemia of low parasite burden in rodent models results from accelerated clearance of uninfected erythrocytes. Blood 107:1192-1199.
21. Ferguson, H. M., M. J. MacKinnon, B. H. Chan, and A. F. Read. 2003. Mosquito mortality and the evolution of malaria virulence. Evolution 57:2792-2804.
22. Fischer, B., B. Taborsky, and U. Dieckmann. 2009. Unexpected patterns of plastic energy allocation in stochastic environments. The American Naturalist 173:E108-E120.
23. Gardner, A., S. E. Reece, and S. A. West. 2003. Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. Journal of Theoretical Biology 223:515-521.
24. Graham, A. L. 2008. Ecological rules governing helminth-microparasite coinfection. Proceedings of the National Academy of Sciences of the United States of America 105:566-570.
25. Hallett, R. L., S. Dunyo, R. Ord, M. Jawara, M. Pinder, A. Randall, A. Alloueche et al. 2006. Chloroquine/sulphadoxine-pyrimethamine for gambian children with malaria: transmission to mosquitoes of multidrug-resistant Plasmodium falciparum. PLoS Clinical Trials 1:e15.
26. Handel, A., A. Yates, S. S. Pilyugin, and R. Antia. 2009. Sharing the burden: antigen transport and rebreaks in immune responses. Journal of the Royal Society Interface 6:447-454.
27. Haydon, D. T., L. Matthews, R. Timms, and N. Colegrave. 2003. Top-down or bottom-up regulation of intra-host blood-stage malaria: do malaria parasites most resemble the dynamics of prey or predator? Proceedings. Biological Sciences/The Royal Society 270:289-298.
28. Heinze, J., and A. Schrempf. 2012. Terminal investment: individual reproduction of ant queens increases with age. PLoS ONE 7:e35201.
29. Jeffery, G. M., and D. E. Eyles. 1955. Infectivity to mosquitoes of Plasmodium falciparum as related to gametocyte density and duration of infection. American Journal of Tropical Medicine and Hygiene 4:781-789.
30. Koella, J. C., and R. Antia. 1995. Optimal pattern of replication and transmission for parasites with 2 stages in their life-cycle. Theoretical Population Biology 47:277-291.
31. Mackinnon, M. J., and A. F. Read. 1999. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53:689-703.
32. Mackinnon, M. J., and A. F. Read. 2003. The effects of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology 126:103-112.
33. Mackinnon, M. J., A. Bell, and A. F. Read. 2005. The effects of mosquito transmission and population bottlenecking on virulence, multiplication rate and rosetting in rodent malaria. International Journal for Parasitology 35:145-153.
34. McNamara, J. M., and A. I. Houston. 1996. State-dependent life histories. Nature 380:215-221.
35. Mideo, N., and T. Day. 2008. On the evolution of reproductive restraint in malaria. Proceedings of the Royal Society of London. Series B, Biological Sciences 275:1217-1224.
36. Mideo, N., and S. E. Reece. 2012. Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiology 7:17-24.
37. Mideo, N., V. C. Barclay, B. H. Chan, N. J. Savill, A. F. Read, and T. Day. 2008. Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. The American naturalist 172:214-238.
38. Mitri, C., I. Thiery, C. Bourgouin, and R. E. Paul. 2009. Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proceedings. Biological Sciences/The Royal Society 276:3721-3726.
39. Nacher, M., P. Singhasivanon, U. Silachamroon, S. Treeprasertsuk, T. Tosukhowong, S. Vannaphan, F. Gay et al. 2002. Decreased hemoglobin concentrations, hyperparasitemia, and severe malaria are associated with increased Plasmodium falciparum gametocyte carriage. Journal of Parasitology 88:97-101.
40. O'Donnell, A. J., P. Schneider, H. G. McWatters, and S. E. Reece. 2011. Fitness costs of disrupting circadian rhythms in malaria parasites. Proceedings. Biological Sciences/The Royal Society 278:2429-2436.
41. Paul, A., J. Kuester, and D. Podzuweit. 1993. Reproductive senescence and terminal investment in female Barbary macaques (Macaca sylvanus) at Salem. International Journal of Primatology 14:105-124.
42. Paul, R. E., T. N. Coulson, A. Raibaud, and P. T. Brey. 2000. Sex determination in malaria parasites. Science 287:128-131.
43. Paul, R. E. L., F. Ariey, and V. Robert. 2003. The evolutionary ecology of Plasmodium. Ecology Letters 6:866-880.
44. Paul, R. E., S. Bonnet, C. Boudin, T. Tchuinkam, and V. Robert. 2007. Age-structured gametocyte allocation links immunity to epidemiology in malaria parasites. Malaria journal 6:123.
45. Piper, K. P., R. E. Hayward, M. J. Cox, and K. P. Day. 1999. Malaria transmission and naturally acquired immunity to PfEMP-1. Infection and Immunity 67:6369-6374.
46. Pollitt, L. C., P. MacGregor, K. Matthews, and S. E. Reece. 2011a. Malaria and trypanosome transmission: different parasites, same rules? Trends in Parasitology 27:197-203.
47. Pollitt, L. C., N. Mideo, D. R. Drew, P. Schneider, N. Colegrave, and S. E. Reece. 2011b. Competition and the evolution of reproductive restraint in malaria parasites. The American Naturalist 177:358-367.
48. Price, R., F. Nosten, J. A. Simpson, C. Luxemburger, L. Phaipun, F. ter Kuile, M. van Vugt et al. 1999. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. American Journal of Tropical Medicine and Hygiene 60:1019-1023.
49. Ramiro, R. S., J. Alpedrinha, L. Carter, A. Gardner, and S. E. Reece. 2011. Sex and death: the effects of innate immune factors on the sexual reproduction of malaria parasites. PLOS Pathog 7: e1001309.
50. Reece, S. E., A. B. Duncan, S. A. West, and A. F. Read. 2005. Host cell preference and variable transmission strategies in malaria parasites. Proceedings of the Royal Society of London. Series B, Biological Sciences 272:511-517.
51. Reece, S. E., D. R. Drew, and A. Gardner. 2008. Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453:609-614.
52. Reece, S. E., R. S. Ramiro, and D. H. Nussey. 2009. Plastic parasites: sophisticated strategies for survival and reproduction? Evolutionary applications 2:11-23.
53. Reece, S. E., E. Ali, P. Schneider, and H. A. Babiker. 2010. Stress, drugs and the evolution of reproductive restraint in malaria parasites. Proceedings of the Royal Society of London. Series B, Biological Sciences 277:3123-3129.
54. Roff, D. A. 1992. The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York.
55. Schall, J. J. 2000. Transmission success of the malaria parasite Plasmodium mexicanum into its vector: role of gametocyte density and sex ratio. Parasitology 121(Pt 6):575-580.
56. Schofield, L., and G. E. Grau. 2005. Immunological processes in malaria pathogenesis. Nature Reviews Immunology 5:722-735.
57. von Seidlein, L., C. Drakeley, B. Greenwood, G. Walraven, and G. Targett. 2001. Risk factors for gametocyte carriage in Gambian children. American Journal of Tropical Medicine and Hygiene 65:523-527.
58. Silvestrini, F., P. Alano, and J. L. Williams. 2000. Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121:465-471.
59. Smith, T. G., P. Lourenco, R. Carter, D. Walliker, and L. C. Ranford-Cartwright. 2000. Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology 121:127-133.
60. Stearns, S. C. 1992. The Evolution of Life Histories. Oxford University Press, New York.
61. Taylor, L. H., and A. F. Read. 1997. Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitology Today 13:135-140.
62. Taylor, L. H., D. Walliker, and A. F. Read. 1997. Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proceedings. Biological Sciences/The Royal Society 264:927-935.
63. Trager, W., and G. S. Gill. 1992. Enhanced gametocyte formation in young erythrocytes by Plasmodium falciparum in vitro. Journal of Protozoology 39:429-432.
64. Trager, W., G. S. Gill, C. Lawrence, and R. L. Nagle. 1999. Plasmodium falciparum: enhanced gametocyte formation in vitro in reticulocyte-rich blood. Experimental Parasitology 91:115-118.
65. Williams, G. C. 1966. Natural selection, costs of reproduction, and a refinement of Lack's principle. The American Naturalist 100:687-690.