1932

Abstract

malaria remains a devastating public health problem. Recent discoveries have shed light on the origin and evolution of parasites and their interactions with their vertebrate and mosquito hosts. malaria originated in Africa from a single horizontal transfer between an infected gorilla and a human, and became global as the result of human migration. Today, malaria is transmitted worldwide by more than 70 different anopheline mosquito species. Recent studies indicate that the mosquito immune system can be a barrier to malaria transmission and that the gene allows the parasite to evade mosquito immune detection. Here, we review the origin and globalization of and integrate this history with analysis of the biology, evolution, and dispersal of the main mosquito vectors. This new perspective broadens our understanding of population structure and the dispersal of important parasite genetic traits.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120215-035211
2016-11-23
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/genet/50/1/annurev-genet-120215-035211.html?itemId=/content/journals/10.1146/annurev-genet-120215-035211&mimeType=html&fmt=ahah

Literature Cited

  1. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L. 1.  et al. 2000. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 17:1467–82 [Google Scholar]
  2. Anthony TG, Polley SD, Vogler AP, Conway DJ. 2.  2007. Evidence of non-neutral polymorphism in Plasmodium falciparum gamete surface protein genes Pfs47 and Pfs48/45. Mol. Biochem. Parasitol. 156:117–23 [Google Scholar]
  3. Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC. 3.  et al. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505:50–55 [Google Scholar]
  4. Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P. 4.  et al. 1994. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109:4413–21 [Google Scholar]
  5. Barillas-Mury C, Kumar S. 5.  2005. Plasmodium-mosquito interactions: a tale of dangerous liaisons. Cell Microbiol. 7:1539–45 [Google Scholar]
  6. Barry AE, Leliwa-Sytek A, Tavul L, Imrie H, Migot-Nabias F. 6.  et al. 2007. Population genomics of the immune evasion (var) genes of Plasmodium falciparum. PLOS Pathog. 3:e34 [Google Scholar]
  7. Baton LA, Ranford-Cartwright LC. 7.  2012. Ookinete destruction within the mosquito midgut lumen explains Anopheles albimanus refractoriness to Plasmodium falciparum (3D7A) oocyst infection. Int. J. Parasitol. 42:249–58 [Google Scholar]
  8. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP. 8.  et al. 2004. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116:661–70 [Google Scholar]
  9. Brackney DE, Schirtzinger EE, Harrison TD, Ebel GD, Hanley KA. 9.  2015. Modulation of flavivirus population diversity by RNA interference. J. Virol. 89:4035–39 [Google Scholar]
  10. Carter R, Mendis KN. 10.  2002. Evolutionary and historical aspects of the burden of malaria. Clin. Microbiol. Rev. 15:564–94 [Google Scholar]
  11. Chang HH, Moss EL, Park DJ, Ndiaye D, Mboup S. 11.  et al. 2013. Malaria life cycle intensifies both natural selection and random genetic drift. PNAS 110:20129–34 [Google Scholar]
  12. Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J. 12.  et al. 2002. Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P. falciparum malaria. Blood 100:1172–76 [Google Scholar]
  13. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G. 13.  2010. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 34:387–95 [Google Scholar]
  14. Clayton AM, Dong Y, Dimopoulos G. 14.  2014. The Anopheles innate immune system in the defense against malaria infection. J. Innate Immun. 6:169–81 [Google Scholar]
  15. Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ. 15.  2013. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619:246–74 [Google Scholar]
  16. Cohuet A, Harris C, Robert V, Fontenille D. 16.  2010. Evolutionary forces on Anopheles: What makes a malaria vector?. Trends Parasitol 26:130–36 [Google Scholar]
  17. Cohuet A, Osta MA, Morlais I, Awono-Ambene PH, Michel K. 17.  et al. 2006. Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep. 7:1285–89 [Google Scholar]
  18. Conway DJ. 18.  2015. Paths to a malaria vaccine illuminated by parasite genomics. Trends Genet. 31:97–107 [Google Scholar]
  19. Crompton PD, Moebius J, Portugal S, Waisberg M, Hart G. 19.  et al. 2014. Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annu. Rev. Immunol. 32:157–87 [Google Scholar]
  20. Dong Y, Dimopoulos G. 20.  2009. Anopheles fibrinogen–related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J. Biol. Chem. 284:9835–44 [Google Scholar]
  21. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA. 21.  et al. 2010. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. PNAS 107:10561–66 [Google Scholar]
  22. 22. Emory Univ 2016. Voyages, The Trans-Atlantic Slave Trade Database. Atlanta, GA: Emory Univ http://www.slavevoyages.org
  23. Enderes C, Kombila D, Dal-Bianco M, Dzikowski R, Kremsner P, Frank M. 23.  2011. Var gene promoter activation in clonal Plasmodium falciparum isolates follows a hierarchy and suggests a conserved switching program that is independent of genetic background. J. Infect. Dis. 204:1620–31 [Google Scholar]
  24. Escalante AA, Freeland DE, Collins WE, Lal AA. 24.  1998. The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. PNAS 95:8124–29 [Google Scholar]
  25. Flint J, Harding RM, Boyce AJ, Clegg JB. 25.  1998. The population genetics of the haemoglobinopathies. Bailliere's Clin. Haematol. 11:1–51 [Google Scholar]
  26. Fontaine MC, Pease JB, Steele A, Waterhouse RM, Neafsey DE. 26.  et al. 2015. Extensive introgression in a malaria vector species complex revealed by phylogenomics. Science 347:1258524 [Google Scholar]
  27. Frank M, Dzikowski R, Amulic B, Deitsch K. 27.  2007. Variable switching rates of malaria virulence genes are associated with chromosomal position. Mol. Microbiol. 64:1486–98 [Google Scholar]
  28. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C. 28.  et al. 2000. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407:1018–22 [Google Scholar]
  29. Grieco JP, Achee NL, Roberts DR, Andre RG. 29.  2005. Comparative susceptibility of three species of Anopheles from Belize, Central America, to Plasmodium falciparum (NF-54). J. Am. Mosq. Control Assoc. 21:279–90 [Google Scholar]
  30. Han YS, Barillas-Mury C. 30.  2002. Implications of Time Bomb model of ookinete invasion of midgut cells. Insect Biochem. Mol. Biol. 32:1311–16 [Google Scholar]
  31. Han YS, Thompson J, Kafatos FC, Barillas-Mury C. 31.  2000. Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J. 19:6030–40 [Google Scholar]
  32. Harbach RE. 32.  2013. The phylogeny and classification of Anopheles. Anopheles Mosquitoes—New Insights into Malaria Vectors S Manguin Rijeka, Croat.: InTech. [Google Scholar]
  33. Hedrick PW. 33.  2011. Population genetics of malaria resistance in humans. Heredity 107:283–304 [Google Scholar]
  34. Hill AV. 34.  1992. Molecular epidemiology of the thalassaemias (including haemoglobin E). Bailliere's Clin. Haematol. 5:209–38 [Google Scholar]
  35. Hill WG, Babiker HA, Ranford-Cartwright LC, Walliker D. 35.  1995. Estimation of inbreeding coefficients from genotypic data on multiple alleles, and application to estimation of clonality in malaria parasites. Genet. Res. 65:53–61 [Google Scholar]
  36. Hume JC, Hamilton H III, Lee KL, Lehmann T. 36.  2011. Susceptibility of Anopheles stephensi to Plasmodium gallinaceum: a trait of the mosquito, the parasite, and the environment. PLOS ONE 6:e20156 [Google Scholar]
  37. Hume JC, Tunnicliff M, Ranford-Cartwright LC, Day KP. 37.  2007. Susceptibility of Anopheles gambiae and Anopheles stephensi to tropical isolates of Plasmodium falciparum. Malar. J. 6:139 [Google Scholar]
  38. Jaramillo-Gutierrez G, Rodrigues J, Ndikuyeze G, Povelones M, Molina-Cruz A, Barillas-Mury C. 38.  2009. Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes. BMC Microbiol. 9:154 [Google Scholar]
  39. Joy DA, Feng X, Mu J, Furuya T, Chotivanich K. 39.  et al. 2003. Early origin and recent expansion of Plasmodium falciparum. Science 300:318–21 [Google Scholar]
  40. Joy DA, Gonzalez-Ceron L, Carlton JM, Gueye A, Fay M. 40.  et al. 2008. Local adaptation and vector-mediated population structure in Plasmodium vivax malaria. Mol. Biol. Evol. 25:1245–52 [Google Scholar]
  41. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO. 41.  et al. 2007. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genom. 8:45 [Google Scholar]
  42. Kumar S, Gupta L, Han YS, Barillas-Mury C. 42.  2004. Inducible peroxidases mediate nitration of Anopheles midgut cells undergoing apoptosis in response to Plasmodium invasion. J. Biol. Chem. 279:53475–82 [Google Scholar]
  43. Laporta GZ, Burattini MN, Levy D, Fukuya LA, de Oliveira TM. 43.  et al. 2015. Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?. Malar. J. 14:181 [Google Scholar]
  44. Lefèvre T, Vantaux A, Dabiré KR, Mouline K, Cohuet A. 44.  2013. Non-genetic determinants of mosquito competence for malaria parasites. PLOS Pathog. 9:e1003365 [Google Scholar]
  45. Li J, Collins WE, Wirtz RA, Rathore D, Lal A, McCutchan TF. 45.  2001. Geographic subdivision of the range of the malaria parasite Plasmodium vivax. Emerg. Infect. Dis. 7:35–42 [Google Scholar]
  46. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD. 46.  et al. 2010. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467:420–25 [Google Scholar]
  47. Livingstone FB. 47.  1958. The distribution of the sickle cell gene in Liberia. Am. J. Hum. Genet. 10:33–41 [Google Scholar]
  48. Luckhart S, Vodovotz Y, Cui L, Rosenberg R. 48.  1998. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. PNAS 95:5700–5 [Google Scholar]
  49. Machado RL, Povoa MM, Calvosa VS, Ferreira MU, Rossit AR. 49.  et al. 2004. Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J. Infect. Dis. 190:1547–55 [Google Scholar]
  50. Makanga B, Yangari P, Rahola N, Rougeron V, Elguero E, Boundenga L. 50.  et al. 2016. Ape malaria transmission and potential for ape-to-human transfers in Africa. PNAS 113:5329–34 [Google Scholar]
  51. Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J. 51.  et al. 2012. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487:375–79 [Google Scholar]
  52. Mitri C, Jacques J-C, Thiery I, Riehle MM, Xu J. 52.  et al. 2009. Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLOS Pathog 5:e1000576 [Google Scholar]
  53. Molina-Cruz A, Barillas-Mury C. 53.  2014. The remarkable journey of adaptation of the Plasmodium falciparum malaria parasite to New World anopheline mosquitoes. Mem. Inst. Oswaldo Cruz 109:662–67 [Google Scholar]
  54. Molina-Cruz A, Barillas-Mury C. 54.  2016. Mosquito vectors of ape malarias: another piece of the puzzle. PNAS 113:5153–54 [Google Scholar]
  55. Molina-Cruz A, Canepa GE, Kamath N, Pavlovic NV, Mu J. 55.  et al. 2015. Plasmodium evasion of mosquito immunity and global malaria transmission: the lock-and-key theory. PNAS 112:15178–83 [Google Scholar]
  56. Molina-Cruz A, Dejong RJ, Ortega C, Haile A, Abban E. 56.  et al. 2012. Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. PNAS 109:1957–62 [Google Scholar]
  57. Molina-Cruz A, Garver LS, Alabaster A, Bangiolo L, Haile A. 57.  et al. 2013. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340:984–87 [Google Scholar]
  58. Moreno M, Marinotti O, Krzywinski J, Tadei WP, James AA. 58.  et al. 2010. Complete mtDNA genomes of Anopheles darlingi and an approach to anopheline divergence time. Malar. J. 9:127 [Google Scholar]
  59. Morlais I, Nsango SE, Toussile W, Abate L, Annan Z. 59.  et al. 2015. Plasmodium falciparum mating patterns and mosquito infectivity of natural isolates of gametocytes. PLOS ONE 10:e0123777 [Google Scholar]
  60. Mu J, Awadalla P, Duan J, McGee KM, Joy DA. 60.  et al. 2005. Recombination hotspots and population structure in Plasmodium falciparum. PLOS Biol 3:e335 [Google Scholar]
  61. Mu J, Duan J, Makova KD, Joy DA, Huynh CQ. 61.  et al. 2002. Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 418:323–26 [Google Scholar]
  62. Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P. 62.  et al. 2008. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol. 9:R171 [Google Scholar]
  63. Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA. 63.  et al. 2015. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes. Science 347:1258522 [Google Scholar]
  64. Nerlich AG, Schraut B, Dittrich S, Jelinek T, Zink AR. 64.  2008. Plasmodium falciparum in ancient Egypt. Emerg. Infect. Dis. 14:1317–19 [Google Scholar]
  65. Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RN. 65.  et al. 2011. Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol. Ecol. 20:1049–61 [Google Scholar]
  66. Nsango SE, Abate L, Thoma M, Pompon J, Fraiture M. 66.  et al. 2012. Genetic clonality of Plasmodium falciparum affects the outcome of infection in Anopheles gambiae. Int. J. Parasitol. 42:589–95 [Google Scholar]
  67. Olago DO. 67.  2001. Vegetation changes over palaeo-time scales in Africa. Clim. Res. 17:105–21 [Google Scholar]
  68. Oliveira de Almeida G, Lieberman J, Barillas-Mury C. 68.  2012. Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 335:856–59 [Google Scholar]
  69. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C. 69.  et al. 2009. A new malaria agent in African hominids. PLOS Pathog. 5:e1000446 [Google Scholar]
  70. Osta MA, Christophides GK, Kafatos FC. 70.  2004. Effects of mosquito genes on Plasmodium development. Science 303:2030–32 [Google Scholar]
  71. Parmakelis A, Russello MA, Caccone A, Marcondes CB, Costa J. 71.  et al. 2008. Historical analysis of a near disaster: Anopheles gambiae in Brazil. Am. J. Trop. Med. Hyg. 78:176–78 [Google Scholar]
  72. Pasvol G, Weatherall DJ, Wilson RJ. 72.  1978. Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 274:701–3 [Google Scholar]
  73. Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC. 73.  et al. 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269:1709–11 [Google Scholar]
  74. Paupy C, Makanga B, Ollomo B, Rahola N, Durand P. 74.  et al. 2013. Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon. PLOS ONE 8:e57294 [Google Scholar]
  75. Perkins SL, Schall JJ. 75.  2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J. Parasitol. 88:972–78 [Google Scholar]
  76. Povelones M, Waterhouse RM, Kafatos FC, Christophides GK. 76.  2009. Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324:258–61 [Google Scholar]
  77. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ. 77.  et al. 2010. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. PNAS 107:1458–63 [Google Scholar]
  78. Prugnolle F, Ollomo B, Durand P, Yalcindag E, Arnathau C. 78.  et al. 2011. African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. PNAS 108:11948–53 [Google Scholar]
  79. Ramirez JL, de Almeida Oliveira G, Calvo E, Dalli J, Colas RA. 79.  et al. 2015. A mosquito lipoxin/lipocalin complex mediates innate immune priming in Anopheles gambiae. Nat. Commun. 6:7403 [Google Scholar]
  80. Ramirez JL, Garver LS, Brayner FA, Alves LC, Rodrigues J. 80.  et al. 2014. The role of hemocytes in Anopheles gambiae antiplasmodial immunity. J. Innate Immun. 6:119–28 [Google Scholar]
  81. Ramphul UN, Garver LS, Molina-Cruz A, Canepa GE, Barillas-Mury C. 81.  2015. Plasmodium falciparum evades mosquito immunity by disrupting JNK-mediated apoptosis of invaded midgut cells. PNAS 112:1273–80 [Google Scholar]
  82. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T. 82.  2010. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes—divide and conquer. PLOS Comput. Biol. 6:e1000933 [Google Scholar]
  83. Rayner JC, Liu W, Peeters M, Sharp PM, Hahn BH. 83.  2011. A plethora of Plasmodium species in wild apes: a source of human infection?. Trends Parasitol. 27:222–29 [Google Scholar]
  84. Read AF. 84.  1994. The evolution of virulence. Trends Microbiol. 2:73–76 [Google Scholar]
  85. Reidenbach KR, Cook S, Bertone MA, Harbach RE, Wiegmann BM, Besansky NJ. 85.  2009. Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evol. Biol. 9:298 [Google Scholar]
  86. Rich SM, Ayala FJ. 86.  1998. The recent origin of allelic variation in antigenic determinants of Plasmodium falciparum. Genetics 150:515–17 [Google Scholar]
  87. Rich SM, Leendertz FH, Xu G, Lebreton M, Djoko CF. 87.  et al. 2009. The origin of malignant malaria. PNAS 106:14902–7 [Google Scholar]
  88. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C. 88.  2010. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329:1353–55 [Google Scholar]
  89. Salamini F, Ozkan H, Brandolini A, Schafer-Pregl R, Martin W. 89.  2002. Genetics and geography of wild cereal domestication in the near east. Nat. Rev. Genet. 3:429–41 [Google Scholar]
  90. Sinden RE, Dawes EJ, Alavi Y, Waldock J, Finney O. 90.  et al. 2007. Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLOS Pathog. 3:e195 [Google Scholar]
  91. Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T. 91.  et al. 2012. A global map of dominant malaria vectors. Parasit. Vectors 5:69 [Google Scholar]
  92. Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH. 92.  et al. 2010. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic precis. Parasit. Vectors 3:72 [Google Scholar]
  93. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE. 93.  et al. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101–10 [Google Scholar]
  94. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA. 94.  et al. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum–infected erythrocytes. Cell 82:89–100 [Google Scholar]
  95. Su XZ, Mu J, Joy DA. 95.  2003. The “Malaria's Eve” hypothesis and the debate concerning the origin of the human malaria parasite Plasmodium falciparum. Microbes Infect. 5:891–96 [Google Scholar]
  96. Tanabe K, Jombart T, Horibe S, Palacpac NM, Honma H. 96.  et al. 2013. Plasmodium falciparum mitochondrial genetic diversity exhibits isolation-by-distance patterns supporting a sub-Saharan African origin. Mitochondrion 13:630–36 [Google Scholar]
  97. Tanabe K, Mita T, Jombart T, Eriksson A, Horibe S. 97.  et al. 2010. Plasmodium falciparum accompanied the human expansion out of Africa. Curr. Biol. 20:1283–89 [Google Scholar]
  98. Taylor SM, Parobek CM, Fairhurst RM. 98.  2012. Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect. Dis. 12:457–68 [Google Scholar]
  99. Tishkoff SA, Varkonyi R, Cahinhinan N, Abbes S, Argyropoulos G. 99.  et al. 2001. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293:455–62 [Google Scholar]
  100. Valencio DA, Vilas JF. 100.  1969. Age of the separation of South America and Africa. Nature 223:1353–54 [Google Scholar]
  101. van Dijk MR, van Schaijk BC, Khan SM, van Dooren MW, Ramesar J. 101.  et al. 2010. Three members of the 6-cys protein family of Plasmodium play a role in gamete fertility. PLOS Pathog. 6:e1000853 [Google Scholar]
  102. van Schaijk BC, van Dijk MR, van de Vegte-Bolmer M, van Gemert GJ, van Dooren MW. 102.  et al. 2006. Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol. Biochem. Parasitol. 149:216–22 [Google Scholar]
  103. Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E. 103.  et al. 2011. Identification and functional validation of the novel antimalarial resistance locus PF10_0355 in Plasmodium falciparum. PLOS Genet. 7:e1001383 [Google Scholar]
  104. Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM. 104.  et al. 2001. Recent origin of Plasmodium falciparum from a single progenitor. Science 293:482–84 [Google Scholar]
  105. Volkman SK, Hartl DL, Wirth DF, Nielsen KM, Choi M. 105.  et al. 2002. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 298:216–18 [Google Scholar]
  106. Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF. 106.  et al. 2007. A genome-wide map of diversity in Plasmodium falciparum. Nat. Genet. 39:113–19 [Google Scholar]
  107. Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS. 107.  et al. 2007. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316:1738–43 [Google Scholar]
  108. White BJ, Lawniczak MKN, Cheng C, Coulibaly MB, Wilson MD. 108.  et al. 2011. Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. PNAS 108:244–49 [Google Scholar]
  109. 109. WHO (World Health Organ.) 2015. World Malaria Report 2015 Geneva, Switz.: World Health Organ.
  110. Wiesenfeld SL. 110.  1967. Sickle-cell trait in human biological and cultural evolution. Development of agriculture causing increased malaria is bound to gene-pool changes causing malaria reduction. Science 157:1134–40 [Google Scholar]
  111. Woodring JL, Higgs S, Beaty BJ. 111.  1996. Natural cycles of vector-borne pathogens. The Biology of Disease Vectors BJ Beaty, WC Marquardt 51–72 Niwot, CO: Univ. Press Colo. [Google Scholar]
  112. Yalcindag E, Elguero E, Arnathau C, Durand P, Akiana J. 112.  et al. 2012. Multiple independent introductions of Plasmodium falciparum in South America. PNAS 109:511–16 [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-035211
Loading
/content/journals/10.1146/annurev-genet-120215-035211
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error