The role of models in translating within-host dynamics to parasite evolution

Parasitology

Volumn 143, Issue 7, 2016, Pages 905-914

  Greischar, Megan A ^a   Reece, Sarah E ^b   Mideo, Nicole ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

fitness; malaria; transmission; Within host ecology

Indexed keywords

ADAPTIVE IMMUNITY; ARTICLE; BIOMASS; DISEASE MODEL; EVOLUTION; GAMETOCYTE; HOST PARASITE INTERACTION; HUMAN; LIFE CYCLE; MALARIA; MATHEMATICAL MODEL; MOLECULAR EVOLUTION; MOSQUITO; NONHUMAN; PARASITE TRANSMISSION; PARASITE VECTOR; PARASITE VIRULENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; ANIMAL; BIOLOGICAL MODEL; PARASITOLOGY; PHYSIOLOGY; RESEARCH; STANDARDS; TRENDS;

ANIMALS; BIOLOGICAL EVOLUTION; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA; MODELS, BIOLOGICAL; RESEARCH;

EID: 84943800295     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182015000815     Document Type: Article

References (91)

1. Alizon, S., Hurford, A., Mideo, N. and van Baalen, M. (2009). Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology 22, 245-259.
2. Anderson, R. and May, R. (1981). The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London: B, Biological Sciences 291, 451-524.
3. Bell, A. S., Huijben, S., Paaijmans, K. P., Sim, D. G., Chan, B. H. K., Nelson, W. A. and Read, F. (2012). Enhanced transmission of drugresistant parasites to mosquitoes following drug treatment in rodent malaria. PLoS ONE 7, e37172.
4. Bottomley, C., Isham, V. and Basáñez, M. G. (2005). Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 131, 417-433.
5. Bousema, T. and Drakeley, C. (2011). Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clinical Microbiology Reviews 24, 377-410.
6. Brancucci, N., Bertschi, N., Zhu, L., Niederwieser, I., Chin, W., Wampfler, R., Freymond, C., Rottmann, M., Felger, I., Bozdech, Z. and Voss, T. (2014). Heterochromatin protein 1 secures survival and transmission of malaria parasites. Cell Host and Microbe 16, 165-176.
7. Bruce, M. C., Alano, P., Duthie, S. and Carter, R. (1990). Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology 100, 191-200.
8. Bruce, M. C., Donnelly, C. A., Packer, M., Lagog, M., Gibson, N., Narara, A., Walliker, D., Alpers, M. P. and Day, K. P. (2000). Ageand species-specific duration of infection in asymptomatic malaria infections in Papua New Guinea. Parasitology 121, 247-256.
9. Cameron, A., Reece, S. E., Drew, D. R., Haydon, D. T. and Yates, A. J. (2012). Plasticity in transmission strategies of the malaria parasite, Plasmodium chabaudi: environmental and genetic effects. Evolutionary Applications 6, 365-376.
10. Carter, R., Gwadz, R. W. and Green, I. (1979). Plasmodium gallinaceum: transmission-blocking immunity in chickens II. The effect of antigamete antibodies in vitro and in vivo and their elaboration during infection. Experimental Parasitology 208, 194-208.
11. Carter, L. M., Kafsack, B. F. C., Llinás, M., Mideo, N., Pollitt, L. C. and Reece, S. E. (2013). Stress and sex in malaria parasites: why does commitment vary? Evolution, Medicine, and Public Health 1, 135-147.
12. Chang, H.-H. and Hartl, D. L. (2015). Recurrent bottlenecks in the malaria life cycle obscure signals of positive selection. Parasitology 142, S98-S107.
13. Chang, H.-H., Moss, E. L., Park, D. J., Ndiaye, D., Mboup, S., Volkman, S. K., Sabeti, P. C., Wirth, D. F., Neafsey, D. E. and Hartl, D. L. (2013). Malaria life cycle intensifies both natural selection and random genetic drift. Proceedings of the National Academy of Sciences of the United States of America 110, 20129-20134.
14. Chao, L., Hanley, K. A., Burch, C. L., Dahlberg, C. and Turner, P. E. (2000). Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Quarterly Review of Biology 75, 261-275.
15. Chen, Q., Fernandez, V., Sundström, A., Schlichtherle, M., Datta, S., Hagblom, P. and Wahlgren, M. (1998). Developmental selection of var gene expression in Plasmodium falciparum. Nature 394, 392-395.
16. Coleman, B. I., Skillman, K. M., Jiang, R. H., Childs, L. M., Altenhofen, L. M., Ganter, M., Leung, Y., Goldowitz, I., Kafsack, B. F., Marti, M., Llinás, M., Buckee, C. O. and Duraisingh, M. T. (2014). A Plasmodium falciparum histone deacetylase regulates antigenic variation and gametocyte conversion. Cell Host and Microbe 16, 177-186.
17. Cornet, S., Nicot, A., Rivero, A. and Gandon, S. (2014). Evolution of plastic transmission strategies in avianmalaria. PLoSPathogens 10, e1004308.
18. Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. and Day, T. (2015). The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology. doi: 10. 1017/ S003118201500092X.
19. Cromer, D., Stark, J. and Davenport, M. P. (2009). Low red cell production may protect against severe anemia during a malaria infection-insights from modeling. Journal of Theoretical Biology 257, 533-542.
20. Cunnington, A. J., Riley, E. M. and Walther,M. (2013). Stuck in a rut? Reconsidering the role of parasite sequestration in severe malaria syndromes. Trends in Parasitology 29, 585-592.
21. Dawes, E. J., Churcher, T. S., Zhuang, S., Sinden, R. E. and Basáñez, M.-G. (2009). Anopheles mortality is both age-and Plasmodiumdensity dependent: implications for malaria transmission. Malaria Journal 8, 228.
22. Day, T., Mideo, N. and Alizon, S. (2008). Why is HIV not vector-borne? Evolutionary Applications 1, 17-27.
23. Day, T., Alizon, S. and Mideo, N. (2011). Bridging scales in the evolution of infectious disease life histories: theory. Evolution 65, 3448-3461.
24. Day, T., Huijben, S. and Read, A. F. (2015). Is selection relevant in the evolutionary emergence of drug resistance? Trends in Microbiology 5, 1-8.
25. Dye, C. and Godfray, H. C. (1993). On sex ratio and inbreeding in malaria parasite populations. Journal of Theoretical Biology 161, 131-134.
26. Eksi, S., Morahan, B. J., Haile, Y., Furuya, T., Jiang, H., Ali, O., Xu, H., Kiattibutr, K., Suri, A., Czesny, B., Adeyemo, A., Myers, T. G., Sattabongkot, J., Su, X.-z. and Williamson, K. C. (2012). Plasmodium falciparum gametocyte development 1 (Pfgdv1) and gametocytogenesis early gene identification and commitment to sexual development. PLoS Pathogens 8, e1002964.
27. Färnert, A., Snounou, G., Rooth, I. and Björkman, A. (1997). Daily dynamics of Plasmodium falciparum subpopulations in asymptomatic children in a holoendemic area. American Journal of Tropical Medicine and Hygiene 56, 538-547.
28. Fenton, A., Viney, M. E. and Lello, J. (2010). Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecology Letters 13, 606-615.
29. Fenton, A., Knowles, S. C. L., Petchey, O. L. and Pedersen, A. B. (2014). The reliability of observational approaches for detecting interspecific parasite interactions: comparison with experimental results. International Journal for Parasitology 44, 437-445.
30. Frank, S. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37-78.
31. Fraser, C., Lythgoe, K., Leventhal, G. E., Shirreff, G., Hollingsworth, T. D., Alizon, S. and Bonhoeffer, S. (2014). Virulence and pathogenesis of HIV-1 infection: an evolutionary perspective. Science 343, 1243727.
32. Gardner, A., Reece, S. and West, S. (2003). Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. Journal of Theoretical Biology 223, 515-521.
33. Gething, P. W., Smith, D. L., Patil, A. P., Tatem, A. J., Snow, R. W. and Hay, S. I. (2010). Climate change and the global malaria recession. Nature 465, 342-345.
34. Gething, P. W., Patil, A. P., Smith,D. L.,Guerra, C. A., Elyazar, I. R. F., Johnston, G. L., Tatem, A. J. and Hay, S. I. (2011). A new world malaria map: Plasmodium falciparum endemicity in 2010. Malaria Journal 10, 378.
35. Glunt, K. D., Thomas, M. B. and Read, A. F. (2011). The effects of age, exposure history and malaria infection on the susceptibility of Anopheles mosquitoes to low concentrations of pyrethroid. PLoS ONE 6, e24968.
36. Greischar, M. A., Read, A. F. and Bjørnstad, O. N. (2014). Synchrony in malaria infections: how intensifying within-host competition can be adaptive. American Naturalist 183, E36-E48.
37. Hamilton, W. D. (1967). Extraordinary sex ratios. Science 156, 477-488.
38. Huijben, S., Nelson, W. A., Wargo, A. R., Sim, D. G., Drew, D. R. and Read, A. F. (2010). Chemotherapy, within-host ecology and the fitness of drug-resistant malaria parasites. Evolution 64, 2952-2968.
39. Huijben, S., Bell, A. S., Sim, D. G., Tomasello, D., Mideo, N., Day, T. and Read, A. F. (2013). Aggressive chemotherapy and the selection of drug resistant pathogens. PLoS Pathogens 9, e1003578.
40. Jafari-Guemouri, S., Boudin, C., Fievet, N., Ndiaye, P. and Deloron, P. (2006). Plasmodium falciparum genotype population dynamics in asymptomatic children from Senegal. Microbes and Infection 8, 1663-1670.
41. Kaestli, M., Cortes, A., Lagog, M., Ott, M. and Beck, H.-P. (2004). Longitudinal assessment of Plasmodium falciparum var gene transcription in naturally infected asymptomatic children in Papua New Guinea. Journal of Infectious Diseases 189, 1942-1951.
42. King, A. A., Shrestha, S., Harvill, E. T. and Bjørnstad, O. N. (2009). Evolution of acute infections and the invasion-persistence trade-off. American Naturalist 173, 446-455.
43. Klein, E. Y., Smith, D. L., Laxminarayan, R. and Levin, S. (2012). Superinfection and the evolution of resistance to antimalarial drugs. Proceedings of the Royal Society B: Biological Sciences 279, 3834-3842.
44. Klein, E. Y., Graham, A. L., Llinás, M. and Levin, S. (2014). Cross-reactive immune responses as primary drivers of malaria chronicity. Infection and Immunity 82, 140-151.
45. Koella, J. C. and Antia, R. (1995). Optimal pattern of replication and transmission for parasites with two stages in their life cycle. Theoretical Population Biology 47, 277-291.
46. Koella, J. C., Lynch, P. A., Thomas, M. B. and Read, A. F. (2009). Towards evolution-proof malaria control with insecticides. Evolutionary Applications 2, 469-480.
47. Landau, I. and Boulard, C. (1978). Life cycles and morphology. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W. ), pp. 53-84. Academic Press Inc., New York.
48. Lessler, J., Edmunds, W., Halloran, M., Hollingsworth, T. and Lloyd, A. (2015). Seven challenges for model-driven data collection in experimental and observational studies. Epidemics, 10, 78-82. doi: 10. 1016/j. epidem. 2014. 12. 002.
49. Lynch, P. A., Grimm, U., Thomas, M. B. and Read, A. F. (2012). Prospective malaria control using entomopathogenic fungi: comparative evaluation of impact on transmission and selection for resistance. Malaria Journal 11, 383.
50. MacGregor, P., Ször, B., Savill, N. J. and Matthews, K. R. (2012). Trypanosomal immune evasion, chronicity and transmission: an elegant balancing act. Nature Reviews Microbiology 10, 431-438.
51. May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal society of London. Series B. Biological sciences 219, 281-313.
52. Metcalf, C. J. E., Graham, A. L., Huijben, S., Barclay, V. C., Long, G. H., Grenfell, B. T., Read, A. F. and Bjørnstad, O. N. (2011). Partitioning regulatory mechanisms of within-host malaria dynamics using the effective propagation number. Science 333, 984-988.
53. Metcalf, C. J. E., Long, G. H., Mideo, N., Forester, J. D., Bjørnstad, O. N. and Graham, A. L. (2012). Revealing mechanisms underlying variation in malaria virulence: effective propagation and host control of uninfected red blood cell supply. Journal of the Royal Society, Interface 9, 2804-2813.
54. Mideo, N. and Day, T. (2008). On the evolution of reproductive restraint in malaria. Proceedings of the Royal Society B: Biological Sciences 275, 1217-1224.
55. Mideo, N., Nelson, W. A., Reece, S. E., Bell, A. S., Read, A. F. and Day, T. (2011a). Bridging scales in the evolution of infectious disease life histories: application. Evolution 65, 3298-3310.
56. Mideo, N., Savill, N. J., Chadwick, W., Schneider, P., Read, A. F., Day, T. and Reece, S. E. (2011b). Causes of variation in malaria infection dynamics: insights from theory and data. American Naturalist 178, E174-E188.
57. Miller, L. H., Good, M. F. and Milon, G. (1994). Malaria pathogenesis. Science 264, 1878-1883.
58. Miller, L. H., Baruch, D. I., Marsh, K. and Doumbo, O. K. (2002). The pathogenic basis of malaria. Nature 415, 673-679.
59. Mitri, C., Thiery, I., Bourgouin, C. and Paul, R. E. L. (2009). Densitydependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proceedings of the Royal Society B: Biological Sciences 276, 3721-3726.
60. Morahan, B. and Garcia-Bustos, J. (2014). Kinase signalling in Plasmodium sexual stages and interventions to stop malaria transmission. Molecular and Biochemical Parasitology 193, 23-32.
61. Neal, A. T. and Schall, J. J. (2010). Gametocyte sex ratio in single-clone infections of the malaria parasite Plasmodium mexicanum. Parasitology 137, 1851-1859.
62. Nee, S., West, S. A. and Read, A. F. (2002). Inbreeding and parasite sex ratios. Proceedings of the Royal Society B: Biological Sciences 269, 755-760.
63. Paul, R. E., Packer, M. J., Walmsley, M., Lagog, M., Ranford-Cartwright, L. C., Paru, R. and Day, K. P. (1995). Mating patterns in malaria parasite populations of Papua New Guinea. Science 269, 1709-1711.
64. Paul, R. E. L., Ariey, F. and Robert, V. (2003). The evolutionary ecology of Plasmodium. Ecology Letters 6, 866-880.
65. Paul, R. E. L., Bonnet, S., Boudin, C., Tchuinkam, T. and Robert, V. (2007). Aggregation in malaria parasites places limits on mosquito infection rates. Infection, Genetics and Evolution 7, 577-586.
66. Pollitt, L. C., Colegrave, N., Khan, S. M., Sajid, M. and Reece, S. E. (2010). Investigating the evolution of apoptosis in malaria parasites: the importance of ecology. Parasites and Vectors 3, 105.
67. Pollitt, L. C., MacGregor, P., Matthews, K. and Reece, S. E. (2011a). Malaria and trypanosome transmission: different parasites, same rules? Trends in Parasitology 27, 197-203.
68. Pollitt, L. C., Mideo, N., Drew, D. R., Schneider, P., Colegrave, N. and Reece, S. E. (2011b). Competition and the evolution of reproductive restraint in malaria parasites. American Naturalist 177, 358-367.
69. Pollitt, L. C., Churcher, T. S., Dawes, E. J., Khan, S. M., Sajid, M., Basáñez, M.-G., Colegrave, N. and Reece, S. E. (2013). Costs of crowding for the transmission of malaria parasites. Evolutionary Applications 6, 617-629.
70. Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3-S11.
71. Ramiro,R. S., Alpedrinha, J., Carter, L., Gardner, A. and Reece, S. E. (2011). Sex and death: the effects of innate immune factors on the sexual reproduction of malaria parasites. PLoS Pathogens 7, e1001309.
72. Read, A. F. and Thomas, M. B. (2009). Mosquitoes cut short. Science 323, 51-52.
73. Read, A. F., Narara, A., Nee, S., Keymer, A. E. and Day, K. P. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, 387-395.
74. Read, A. F., Anwar, M., Shutler, D. and Nee, S. (1995). Sex allocation and population structure in malaria and related parasitic protozoa. Proceedings of the Royal Society B: Biological Sciences 260, 359-363.
75. Recker, M., Buckee, C. O., Serazin, A., Kyes, S., Pinches, R., Christodoulou, Z., Springer, A. L., Gupta, S. and Newbold, C. I. (2011). Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PLoS Pathogens 7, e1001306.
76. Reece, S. E., Duncan, A. B., West, S. A. and Read, A. F. (2003). Sex ratios in the rodent malaria parasite, Plasmodium chabaudi. Parasitology 127, 419-425.
77. Reece, S. E., Drew, D. R. and Gardner, A. (2008). Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453, 609-614.
78. Reece, S. E., Pollitt, L. C., Colegrave, N. and Gardner, A. (2011). The meaning of death: evolution and ecology of apoptosis in protozoan parasites. PLoS Pathogens 7, e1002320.
79. Robert, V., Read, A. F., Essong, J., Tchuinkam, T., Mulder, B., Verhave, J.-P. and Carnevale, P. (1996). Effect of sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 621-624.
80. Scherf, A., Lopez-Rubio, J. J. and Riviere, L. (2008). Antigenic variation in Plasmodium falciparum. Annual Review of Microbiology 62, 445-470.
81. Shutler, D. and Read, A. F. (1998). Local mate competition, and extraordinary and ordinary blood parasite sex ratios. Oikos 82, 417-424.
82. Sinden, R. E., Dawes, E. J., Alavi, Y., Waldock, J., Finney, O., Mendoza, J., Butcher, G. A., Andrews, L., Hill, A. V., Gilbert, S. C. and Basáñez, M.-G. (2007). Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLoS Pathogens 3, 2005-2016.
83. Smith, D. L., McKenzie, F. E., Snow, R. W. and Hay, S. I. (2007). Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biology 5, e42.
84. Smith, T. G., Walliker, D. and Ranford-Cartwright, L. C. (2002). Sexual differentiation and sex determination in the Apicomplexa. Trends in Parasitology 18, 315-323.
85. Snounou, G., Jarra, W. and Preiser, P. R. (2000). Malaria multigene families: the price of chronicity. Parasitology Today 16, 28-30.
86. Sowunmi, A., Gbotosho, G. O., Happi, C. T., Folarin, O. A. and Balogun, S. T. (2009). Population structure of Plasmodium falciparum gametocyte sex ratios in malarious children in an endemic area. Parasitology International 58, 438-443.
87. Talman, A. M., Domarle, O., McKenzie, F. E., Ariey, F. and Robert, V. (2004). Gametocytogenesis: the puberty of Plasmodium falciparum. Malaria Journal 3, 24.
88. Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, New York.
89. West, S. A., Smith, T. G. and Read, A. F. (2000). Sex allocation and population structure in apicomplexan (protozoa) parasites. Proceedings of the Royal Society B: Biological Sciences 267, 257-263.
90. West, S. A., Reece, S. E. and Read, A. F. (2001). Evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites. Trends in Parasitology 17, 525-531.
91. West, S. A., Smith, T. G., Nee, S. and Read, A. F. (2002). Fertility insurance and the sex ratios of malaria and related hemospororin blood parasites. Journal of Parasitology 88, 258-263.