Abstract
Interactions between Plasmodium parasites and their Anopheles vectors are central to the epidemiology of human malaria. This chapter highlights how an evolutionary perspective on Anopheles-Plasmodium interactions can provide important insights into the history, distribution and dynamics of malaria transmission. It focuses on three aspects: (1) the macro-evolutionary history of malaria parasites in relation with their vectors, (2) the micro-evolutionary mechanisms shaping mosquito-parasite interactions and their impact on malaria transmission, and (3) the contribution of evolutionary concepts in the assessment of novel strategies to control malaria. The geographical distribution of diverse anopheline species and populations has played an important role in the past and present distribution of malaria. In particular, speciation processes and genetic differentiation of vectors may have been important drivers of the evolution of human malaria parasites. A full understanding of the epidemiology of malaria also requires careful consideration of the micro-evolutionary relationships between mosquitoes and malaria parasites. Malaria parasites have evolved, for example, to manipulate several parameters of the vector biology that are expected to increase their transmission. Finally, an evolutionary approach is useful for assessing the feasibility of innovative malaria control strategies such as the release of transgenic mosquitoes. Considering the epidemiological feedback and the evolutionary response of wild mosquito and parasite populations is crucial for predicting the evolutionary trajectory of such a control measure. A major challenge for future research is to obtain quantitative, epidemiologically relevant estimates of the critical parameters underlying Anopheles-Plasmodium interactions in natural systems.
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Alphey L, Beard CB, Billingsley P, Coetzee M, Crisanti A, Curtis C, Eggleston P, Godfray C, Hemingway J, Jacobs-Lorena M, James AA, Kafatos FC, Mukwaya LG, Paton M, Powell JR, Schneider W, Scott TW, Sina B, Sinden R, Sinkins S, Spielman A, Toure Y and Collins FH (2002) Malaria control with genetically manipulated insect vectors. Science 298: 119-121.
Alphey L, Nimmo D, O’Connell S and Alphey N (2008) Insect population suppression using engineered insects. Adv Exp Med Biol 627: 93-103.
Alphey N, Bonsall MB and Alphey L (2011) Modeling resistance to genetic control of insects. J Theor Biol 270: 42-55.
Anderson RA, Knols BG and Koella JC (2000) Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology 120 (Pt 4): 329-333.
Anderson RA, Koella JC and Hurd H (1999) The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proc Biol Sci 266: 1729-1733.
Anderson RM and May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, Oxford, UK.
Ayala SC and Lee D (1970) Saurian malaria: development of sporozoites in two species of phlebotomine sandflies. Science 167: 891-892.
Bargielowski I, Alphey L and Koella JC (2011a) Cost of mating and insemination capacity of a genetically modified mosquito Aedes aegypti OX513A compared to its wild type counterpart. PLoS ONE 6: e26086.
Bargielowski I and Koella JC (2009) A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis. PLoS ONE 4: e4676.
Bargielowski I, Nimmo D, Alphey L and Koella JC (2011b) Comparison of life history characteristics of the genetically modified OX513A line and a wild type strain of Aedes aegypti. PLoS ONE 6: e20699.
Billingsley PF and Sinden RE (1997) Determinants of malaria-mosquito specificity. Parasitology Today 13: 297-301.
Boëte C (2009) Anopheles mosquitoes: not just flying malaria vectors… especially in the field. Trends Parasitol 25: 53-55.
Boëte C (2005) Malaria parasites in mosquitoes: laboratory models, evolutionary temptation and the real world. Trends Parasitol 21: 445-447.
Boëte C and Koella JC (2002) A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J 1: 3.
Boëte C and Koella JC (2003) Evolutionary ideas about genetically manipulated mosquitoes and malaria control. Trends Parasitol 19: 32-38.
Boëte C, Paul RE and Koella JC (2004) Direct and indirect immunosuppression by a malaria parasite in its mosquito vector. Proc R Soc Lond B Biol Sci 271: 1611-1615.
Catteruccia F (2007) Malaria vector control in the third millennium: progress and perspectives of molecular approaches. Pest Manag Sci 63: 634-640.
Charlwood JD and Tomas EV (2011) Do developing malaria parasites manipulate their mosquito host? Evidence from infected Anopheles funestus (Giles) from Mozambique. Trans R Soc Trop Med Hyg 105: 352-354.
Chen CH, Huang H, Ward CM, Su JT, Schaeffer LV, Guo M and Hay BA (2007) A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316: 597-600.
Christophides GK (2005) Transgenic mosquitoes and malaria transmission. Cell Microbiol 7: 325-333.
Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffmann JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Muller HM, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, Von Mering C, Xu J, Zheng L, Bork P and Kafatos FC (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298: 159-165.
Cohuet A, Osta MA, Morlais I, Awono-Ambene PH, Michel K, Simard F, Christophides GK, Fontenille D and Kafatos FC (2006) Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep 7: 1285-1289.
Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC and Gwadz RW (1986) Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234: 607-610.
Coluzzi M, Sabatini A, della Torre A, Di Deco MA and Petrarca V (2002) A polytene chromosome analysis of the Anopheles gambiae species complex. Science 298: 1415-1418.
Corby-Harris V, Drexler A, Watkins de Jong L, Antonova Y, Pakpour N, Ziegler R, Ramberg F, Lewis EE, Brown JM, Luckhart S and Riehle MA (2010) Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathog 6: e1001003.
Day JF and Edman JD (1984) Mosquito engorgement on normally defensive hosts depends on host activity patterns. J Med Entomol 21: 732-740.
Dong Y, Manfredini F and Dimopoulos G (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423.
Edman JD, Day JF and Walker ED (1984) Field confirmation of laboratory observations on the differential antimosquito behavior of herons. Condor 86: 91-92.
Ferguson HM and Read AF (2002) Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol 18: 256-261.
Harris AF, Nimmo D, McKemey AR, Kelly N, Scaife S, Donnelly CA, Beech C, Petrie WD and Alphey L (2011) Field performance of engineered male mosquitoes. Nature Biotechnol 29: 1034-1037.
Harris C, Lambrechts L, Rousset F, Abate L, Nsango SE, Fontenille D, Morlais I and Cohuet A (2010) Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog 6.
Harris C, Morlais I, Churcher TS, Awono-Ambene P, Gouagna LC, Dabire RK, Fontenille D and Cohuet A (2012) Plasmodium falciparum produce lower infection intensities in local versus foreign Anopheles gambiae populations. PLoS ONE 7: e30849.
Hill CA, Kafatos FC, Stansfield SK and Collins FH (2005) Arthropod-borne diseases: vector control in the genomics era. Nat Rev Microbiol 3: 262-268.
Hume JC, Lyons EJ and Day KP (2003) Human migration, mosquitoes and the evolution of Plasmodium falciparum. Trends Parasitol 19: 144-149.
Hurd H (2007) Nature or nurture in mosquito resistance to malaria? Trends Parasitol 23: 135-138.
Ito J, Ghosh A, Moreira LA, Wimmer EA and Jacobs-Lorena M (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417: 452-455.
Joy DA, Gonzalez-Ceron L, Carlton JM, Gueye A, Fay M, McCutchan TF and Su XZ (2008) Local adaptation and vector-mediated population structure in Plasmodium vivax malaria. Mol Biol Evol 25: 1245-1252.
Koella JC (1999) An evolutionary view of the interactions between anopheline mosquitoes and malaria parasites. Microbes Infect 1: 303-308.
Koella JC and Boëte C (2003) A model for the coevolution of immunity and immune evasion in vector-borne diseases with implications for the epidemiology of malaria. Am Naturalist 161: 698-707.
Koella JC and Boëte C (2002) A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution 56: 1074-1079.
Koella JC, Rieu L and Paul REL (2002) Stage-specific manipulation of a mosquito’s host-seeking behavior by the malaria parasite Plasmodium gallinaceum. Behavioral Ecology 13: 816-820.
Koella JC, Sorensen FL and Anderson RA (1998) The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae. Proc R Soc Lond B Biol Sci 265: 763-768.
Koella JC and Zaghloul L (2008) Using evolutionary costs to enhance the efficacy of malaria control via genetically manipulated mosquitoes. Parasitology 135: 1489-1496.
Lacroix R, Mukabana WR, Gouagna LC and Koella JC (2005) Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol 3: e298.
Lambrechts L, Chavatte JM, Snounou G and Koella JC (2006a) Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proc Biol Sci 273: 1501-1506.
Lambrechts L, Fellous S and Koella JC (2006b) Coevolutionary interactions between host and parasite genotypes. Trends Parasitol 22: 12-16.
Lambrechts L, Halbert J, Durand P, Gouagna LC and Koella JC (2005) Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar J 4: 3.
Lambrechts L, Koella JC and Boëte C (2008) Can transgenic mosquitoes afford the fitness cost? Trends Parasitol 24: 4-7.
Lambrechts L, Morlais I, Awono-Ambene PH, Cohuet A, Simard F, Jacques JC, Bourgouin C and Koella JC (2007) Effect of infection by Plasmodium falciparum on the melanization immune response of Anopheles gambiae. Am J Trop Med Hyg 76: 475-480.
Lawniczak MK, Emrich SJ, Holloway AK, Regier AP, Olson M, White B, Redmond S, Fulton L, Appelbaum E, Godfrey J, Farmer C, Chinwalla A, Yang SP, Minx P, Nelson J, Kyung K, Walenz BP, Garcia-Hernandez E, Aguiar M, Viswanathan LD, Rogers YH, Strausberg RL, Saski CA, Lawson D, Collins FH, Kafatos FC, Christophides GK, Clifton SW, Kirkness EF and Besansky NJ (2010) Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330: 512-514.
Leonard KJ (1994) Stability of equilibria in a gene-for-gene coevolution model of host-parasite interactions. Phytopathology 84: 70-77.
Levine ND (1988) The protozoan phylum Apicomplexa, 2. CRC Press, Boca Raton, FL, USA.
Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JB, Sanz CM, Morgan DB, Locatelli S, Gonder MK, Kranzusch PJ, Walsh PD, Delaporte E, Mpoudi-Ngole E, Georgiev AV, Muller MN, Shaw GM, Peeters M, Sharp PM, Rayner JC and Hahn BH (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467: 420-425.
Lyimo EO and Koella JC (1992) Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology 104 (Pt 2): 233-237.
Lyimo IN and Ferguson HM (2009) Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol 25: 189-196.
MacDonald G (1957) The epidemiology and control of malaria. Oxford University Press, London, UK.
Mackinnon MJ and Marsh K (2010) The selection landscape of malaria parasites. Science 328: 866-871.
Marrelli MT, Li C, Rasgon JL and Jacobs-Lorena M (2007) Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proc Natl Acad Sci USA 104: 5580-5583.
Marshall JM and Taylor CE (2009) Malaria control with transgenic mosquitoes. PLoS Med 6: e20.
Martinsen ES, Perkins SL and Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47: 261-273.
Meister S, Agianian B, Turlure F, Relogio A, Morlais I, Kafatos FC and Christophides GK (2009) Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 5: e1000542.
Menge DM, Zhong D, Guda T, Gouagna L, Githure J, Beier J and Yan G (2006) Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya. Genetics 173: 235-241.
Michel K, Suwanchaichinda C, Morlais I, Lambrechts L, Cohuet A, Awono-Ambene PH, Simard F, Fontenille D, Kanost MR and Kafatos FC (2006) Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc Natl Acad Sci USA 103: 16858-16863.
Niaré O, Markianos K, Volz J, Oduol F, Toure A, Bagayoko M, Sangare D, Traore SF, Wang R, Blass C, Dolo G, Bouare M, Kafatos FC, Kruglyak L, Toure YT and Vernick KD (2002) Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science 298: 213-216.
Nirmala X and James AA (2003) Engineering Plasmodium-refractory phenotypes in mosquitoes. Trends Parasitol 19: 384-387.
Obbard DJ, Callister DM, Jiggins FM, Soares DC, Yan G and Little TJ (2008) The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae. BMC Evol Biol 8: 274.
Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF and Thomas MB (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107: 15135-15139.
Parmakelis A, Slotman MA, Marshall JC, Awono-Ambene PH, Antonio-Nkondjio C, Simard F, Caccone A and Powell JR (2008) The molecular evolution of four anti-malarial immune genes in the Anopheles gambiae species complex. BMC Evol Biol 8: 79.
Pike AD, Cirimotich CM and Dimopoulos G (2013) Impact of transgenic immune deployment on mosquito fitness. In: Koenraadt CJM and Takken W (eds.) Ecology of vector-parasite interactions. Ecology and control of vector-borne diseases, Vol. 3. Wageningen Academic Publishers, Wageningen, the Netherlands, pp. 19-33.
Prugnolle F, Durand P, Jacob K, Razakandrainibe F, Arnathau C, Villarreal D, Rousset F, de Meeus T and Renaud F (2008) A comparison of Anopheles gambiae and Plasmodium falciparum genetic structure over space and time. Microbes Infect 10: 269-275.
Prugnolle F, Durand P, Ollomo B, Duval L, Ariey F, Arnathau C, Gonzalez JP, Leroy E and Renaud F (2011) A fresh look at the origin of Plasmodium falciparum, the most malignant malaria agent. PLoS Pathog 7: e1001283.
Rich SM, Licht MC, Hudson RR and Ayala FJ (1998) Malaria’s eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci USA 95: 4425-4430.
Riehle MM, Guelbeogo WM, Gneme A, Eiglmeier K, Holm I, Bischoff E, Garnier T, Snyder GM, Li X, Markianos K, Sagnon N and Vernick KD (2011) A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 331: 596-598.
Riehle MM, Markianos K, Niare O, Xu J, Li J, Toure AM, Podiougou B, Oduol F, Diawara S, Diallo M, Coulibaly B, Ouatara A, Kruglyak L, Traore SF and Vernick KD (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577-579.
Rossignol PA, Ribeiro JM and Spielman A (1984) Increased intradermal probing time in sporozoite-infected mosquitoes. Am J Trop Med Hyg 33: 17-20.
Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50: 529-551.
Sinkins SP and Gould F (2006) Gene drive systems for insect disease vectors. Nat Rev Genet 7: 427-435.
Slotman MA, Parmakelis A, Marshall JC, Awono-Ambene PH, Antonio-Nkondjo C, Simard F, Caccone A and Powell JR (2007) Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis. PLoS ONE 2: e793.
Smith DL, McKenzie FE, Snow RW and Hay SI (2007) Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol 5: e42.
Tanabe K, Mita T, Jombart T, Eriksson A, Horibe S, Palacpac N, Ranford-Cartwright L, Sawai H, Sakihama N, Ohmae H, Nakamura M, Ferreira MU, Escalante AA, Prugnolle F, Bjorkman A, Farnert A, Kaneko A, Horii T, Manica A, Kishino H and Balloux F (2010) Plasmodium falciparum accompanied the human expansion out of Africa. Curr Biol 20: 1283-1289.
Tripet F, Aboagye-Antwi F and Hurd H (2008) Ecological immunology of mosquito-malaria interactions. Trends Parasitol 24: 219-227.
Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M and Miller LH (1995) Plasmodium gallinaceum: a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Experimental Parasitology 80: 583-595.
Vittor AY, Pan W, Gilman RH, Tielsch J, Glass G, Shields T, Sanchez-Lozano W, Pinedo VV, Salas-Cobos E, Flores S and Patz JA (2009) Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg 81: 5-12.
Vlachou D, Schlegelmilch T, Christophides GK and Kafatos FC (2005) Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 15: 1185-1195.
Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM, Choi M, Thakore SS, Day KP, Wirth DF and Hartl DL (2001) Recent origin of Plasmodium falciparum from a single progenitor. Science 293: 482-484.
White BJ, Lawniczak MK, Cheng C, Coulibaly MB, Wilson MD, Sagnon N, Costantini C, Simard F, Christophides GK and Besansky NJ (2010) Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proc Natl Acad Sci USA 108: 244-249.
Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ, Jr, Burt A and Crisanti A (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473: 212-215.
Wise de Valdez MR, Nimmo D, Betz J, Gong HF, James AA, Alphey L and Black WC (2011) Genetic elimination of dengue vector mosquitoes. Proc Natl Acad Sci USA 108: 4772-4775.
Yakob L, Bonsall MB and Yan G (2010) Modelling knowlesi malaria transmission in humans: vector preference and host competence. Malar J 9: 329.
Yassine H and Osta MA (2010) Anopheles gambiae innate immunity. Cell Microbiol 12: 1-9.
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Lambrechts, L., Koella, J.C. (2013). Evolutionary aspects of Anopheles-Plasmodium interactions. In: Ecology of parasite-vector interactions. Ecology and control of vector-borne diseases, vol 3. Wageningen Academic Publishers, Wageningen. https://doi.org/10.3920/978-90-8686-744-8_6
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