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Different distribution of malaria parasite in left and right extremities of vertebrate hosts translates into differences in parasite transmission

  • 1.

    WHO | World malaria report 2019. WHO, https://www.who.int/publications-detail/world-malaria-report-2019.

  • 2.

    Bhatt, S. et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 526, 207–211 (2015).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 3.

    Weill, M. et al. Comparative genomics: Insecticide resistance in mosquito vectors. Nature 423, 136–137 (2003).

    ADS  CAS  PubMed  Google Scholar 

  • 4.

    Ranson, H. & Lissenden, N. Insecticide resistance in African anopheles mosquitoes: A worsening situation that needs urgent action to maintain malaria control. Trends Parasitol. 32, 187–196 (2016).

    CAS  PubMed  Google Scholar 

  • 5.

    Price, R. N. et al. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet Lond. Engl. 364, 438–447 (2004).

    CAS  Google Scholar 

  • 6.

    Ariey, F. et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505, 50–55 (2014).

    ADS  PubMed  Google Scholar 

  • 7.

    Carter, R. Transmission blocking malaria vaccines. Vaccine 19, 2309–2314 (2001).

    CAS  PubMed  Google Scholar 

  • 8.

    Carter, R. & Chen, D. H. Malaria transmission blocked by immunisation with gametes of the malaria parasite. Nature 263, 57 (1976).

    ADS  CAS  PubMed  Google Scholar 

  • 9.

    Doumbo, O. K., Niaré, K., Healy, S. A. & Duffy, I. S. and P. E. Malaria transmission-blocking vaccines: Present status and future perspectives. In: Towards Malaria Elimination-A Leap Forward. IntechOpen. (2018).

  • 10.

    Acquah, F. K., Adjah, J., Williamson, K. C. & Amoah, L. E. Transmission-blocking vaccines: old friends and new prospects. Infect. Immun. 87, e00775–18 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 11.

    Wu, Y., Sinden, R. E., Churcher, T. S., Tsuboi, T. & Yusibov, V. Chapter three – Development of malaria transmission-blocking vaccines: From concept to product. in Advances in Parasitology (eds. Rollinson, D. & Stothard, J. R.) vol. 89 109–152 (Academic Press, 2015).

  • 12.

    Bompard, A. et al. Evaluation of two lead malaria transmission blocking vaccine candidate antibodies in natural parasite-vector combinations. Sci. Rep. 7, 1–9 (2017).

    CAS  Google Scholar 

  • 13.

    Mathias, D. K. et al. A Small molecule glycosaminoglycan mimetic blocks Plasmodium invasion of the mosquito midgut. PLOS Pathog. 9, e1003757 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 14.

    Niu, G. et al. Targeting mosquito FREP1 with a fungal metabolite blocks malaria transmission. Sci. Rep. 5, 14694 (2015).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 15.

    Dong, Y., Manfredini, F. & Dimopoulos, G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5, e1000423 (2009).

    PubMed  PubMed Central  Google Scholar 

  • 16.

    Cirimotich, C. M., Ramirez, J. L. & Dimopoulos, G. Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10, 307–310 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 17.

    Hughes, G. L., Rivero, A. & Rasgon, J. L. Wolbachia can enhance Plasmodium infection in mosquitoes: Implications for malaria control? PLOS Pathog. 10, e1004182 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 18.

    Atkinson, C. T., Woods, K. L., Dusek, R. J., Sileo, L. S. & Iko, W. M. Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected iiwi (Vestiaria coccinea). Parasitology 111(Suppl), S59–69 (1995).

    PubMed  Google Scholar 

  • 19.

    Atkinson, C. T. & Samuel, M. D. Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on apapane Himatione sanguinea. J. Avian Biol. 41, 357–366 (2010).

    Google Scholar 

  • 20.

    Ewen, J. G. et al. Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecol. Lett. 15, 1112–1119 (2012).

    PubMed  Google Scholar 

  • 21.

    Ichimori, K. Correlation of mosquito size, blood meal size and malarial oocyst production. Med. Entomol. Zool. 40, 81–85 (1989).

    Google Scholar 

  • 22.

    Jeffery, G. M. Blood meal volume in Anopheles quadrimaculatus, A. albimanus and Aedes aegypti. Exp. Parasitol. 5, 371–375 (1956).

    CAS  PubMed  Google Scholar 

  • 23.

    Bradley, J. et al. Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density. eLife 7, e34463 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 24.

    Da, D. F. et al. Experimental study of the relationship between Plasmodium gametocyte density and infection success in mosquitoes; implications for the evaluation of malaria transmission-reducing interventions. Exp. Parasitol. 149, 74–83 (2015).

    PubMed  Google Scholar 

  • 25.

    Ouédraogo, A. L. et al. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J. Infect. Dis. 213, 90–99 (2016).

    PubMed  Google Scholar 

  • 26.

    Koepfli, C. & Yan, G. Plasmodium gametocytes in field studies: Do we measure commitment to transmission or detectability? Trends Parasitol. 34, 378–387 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 27.

    Slater, H. C. et al. The temporal dynamics and infectiousness of subpatent Plasmodium falciparum infections in relation to parasite density. Nat. Commun. 10, 1433 (2019).

    ADS  PubMed  PubMed Central  Google Scholar 

  • 28.

    Drew, D. R. & Reece, S. E. 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 (2007).

    CAS  PubMed  Google Scholar 

  • 29.

    Gruenberg, M. et al. qRT-PCR versus IFA-based quantification of male and female gametocytes in low-density Plasmodium falciparum infections and their relevance for transmission. J. Infect. Dis. 221(4), 598–607 (2020).

    CAS  PubMed  Google Scholar 

  • 30.

    O’Meara, W. P., Collins, W. E. & McKenzie, F. E. Parasite prevalence: A static measure of dynamic infections. Am. J. Trop. Med. Hyg. 77, 246–249 (2007).

    PubMed  PubMed Central  Google Scholar 

  • 31.

    Färnert, A. Plasmodium falciparum population dynamics: only snapshots in time? Trends Parasitol. 24, 340–344 (2008).

    PubMed  Google Scholar 

  • 32.

    Schneider, P. et al. Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes. Proc. Biol. Sci. 285, (2018).

  • 33.

    Pigeault, R., Caudron, Q., Nicot, A., Rivero, A. & Gandon, S. Timing malaria transmission with mosquito fluctuations. Evol. Lett. 2, 378–389 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 34.

    Isaïa, J., Rivero, A., Glaizot, O., Christe, P. & Pigeault, R. Last-come, best served? Mosquito biting order and Plasmodium transmission. bioRxiv 031625 (2020).

  • 35.

    Huff, C. G. & Bloom, W. A malarial parasite infecting all blood and blood-forming cells of birds. J. Infect. Dis. 57, 315–336 (1935).

    Google Scholar 

  • 36.

    Janse, C. J. et al. In vitro formation of ookinetes and functional maturity of Plasmodium berghei gametocytes. Parasitology 91, 19–29 (1985).

    PubMed  Google Scholar 

  • 37.

    Douglas, R. G., Amino, R., Sinnis, P. & Frischknecht, F. Active migration and passive transport of malaria parasites. Trends Parasitol. 31, 357–362 (2015).

    PubMed  Google Scholar 

  • 38.

    Boyd, M. F., Stratman-Thomas, W. K. & Kitchen, S. F. On the relative susceptibility of Anopheles quadrimaculatus to Plasmodium vivax and Plasmodium falciparum. Am. J. Trop. Med. Hyg. s1-15, 485–493 (1935).

    Google Scholar 

  • 39.

    Muirhead-Thomson, R. C. & Mercier, E. C. Factors in malaria transmission by Anopheles albimanus in Jamaica. Ann. Trop. Med. Parasitol. 46, 103–116 (1952).

    CAS  PubMed  Google Scholar 

  • 40.

    Smalley, M. E., Abdalla, S. & Brown, J. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans. R. Soc. Trop. Med. Hyg. 75, 103–105 (1981).

    CAS  PubMed  Google Scholar 

  • 41.

    Pritsch, M. et al. Stability of gametocyte-specific Pfs25-mRNA in dried blood spots on filter paper subjected to different storage conditions. Malar. J. 11, 138 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 42.

    Pichon, G., Awono-Ambene, H. P. & Robert, V. High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host. Parasitology 121(Pt 2), 115–120 (2000).

    PubMed  Google Scholar 

  • 43.

    Gaillard, F. O., Boudin, C., Chau, N. P., Robert, V. & Pichon, G. Togetherness among Plasmodium falciparum gametocytes: interpretation through simulation and consequences for malaria transmission. Parasitology 127, 427–435 (2003).

    CAS  PubMed  Google Scholar 

  • 44.

    Sinden, R. E. Sexual development of malarial parasites. in Advances in Parasitology (eds. Baker, J. R. & Muller, R.) vol. 22 153–216 (Academic Press, 1983).

  • 45.

    Ouedraogo, J., Guiguemde, T. & Gbary, A. Etude comparative de la densite parasitaire de Plasmodium falciparum dans le sang capillaire et dans le sang veineux chez des porteurs asymptomatiques (région de Bobo-Dioulasso, Burkina Faso). Médecine D’Afrique Noire 38, 601–605 (1991).

    Google Scholar 

  • 46.

    Njunda, A., Assob, N., Nsagha, S., Mokenyu, M. & Kwenti, E. Comparison of capillary and venous blood using blood film microscopy in the detection of malaria parasites: A hospital based study. Sci. J. Microbiol. 2, 89–94 (2013).

    Google Scholar 

  • 47.

    Kast, K. et al. Evaluation of Plasmodium falciparum gametocyte detection in different patient material. Malar. J. 12, 438 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 48.

    Mischlinger, J. et al. Use of capillary blood samples leads to higher parasitemia estimates and higher diagnostic sensitivity of microscopic and molecular diagnostics of malaria than venous blood samples. J. Infect. Dis. 218, 1296–1305 (2018).

    PubMed  Google Scholar 

  • 49.

    Sandeu, M. M. et al. Do the venous blood samples replicate malaria parasite densities found in capillary blood? A field study performed in naturally-infected asymptomatic children in Cameroon. Malar. J. 16, 345 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 50.

    Lehane, A. et al. Comparison on simultaneous capillary and venous parasite density and genotyping results from children and adults with uncomplicated malaria: a prospective observational study in Uganda. BMC Infect. Dis. 19, 559 (2019).

    PubMed  PubMed Central  Google Scholar 

  • 51.

    Meibalan, E. et al. P. falciparum gametocyte density and infectivity in peripheral blood and skin tissue of naturally infected parasite carriers. J Infect Dis. jiz680 (2019).

  • 52.

    van den Berghe, L., Chardome, M. & Peel, E. Supériorité des préparations de scarification du derme sur les préparations de sang périphérique pour le diagnostic de malaria. Instit Med Trop 9, 553–562 (1952).

    Google Scholar 

  • 53.

    Palmer, A. R. & Strobeck, C. Fluctuating asymmetry analyses revisited. in Developmental instability: causes and consequences 279–319 (2003).

  • 54.

    Rivero, A. & Gandon, S. Evolutionary ecology of avian malaria: Past to present. Trends Parasitol. 34(8), 712–726 (2018).

    PubMed  Google Scholar 

  • 55.

    Pigeault, R. et al. Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology of Plasmodium. Phil Trans R Soc B 370, 20140300 (2015).

    PubMed  Google Scholar 

  • 56.

    Alonso, P. L. et al. A Research agenda to underpin malaria eradication. PLOS Med. 8, e1000406 (2011).

    PubMed  PubMed Central  Google Scholar 

  • 57.

    Dearsly, A. L., Sinden, R. E. & Self, I. A. Sexual development in malarial parasites: gametocyte production, fertility and infectivity to the mosquito vector. Parasitology 100, 359–368 (1990).

    PubMed  Google Scholar 

  • 58.

    Sattabongkot, J., Maneechai, N. & Rosenberg, R. Plasmodium vivax: Gametocyte infectivity of naturally infected Thai adults. Parasitology 102(Pt 1), 27–31 (1991).

    PubMed  Google Scholar 

  • 59.

    Gaye, A. et al. Infectiousness of the human population to Anopheles arabiensis by direct skin feeding in an area hypoendemic for malaria in Senegal. Am. J. Trop. Med. Hyg. 92, 648–652 (2015).

    Google Scholar 

  • 60.

    Ouédraogo, A. L. et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE 4, (2009).

  • 61.

    Morlais, I. et al. Plasmodium falciparum mating patterns and mosquito infectivity of natural isolates of gametocytes. PLOS ONE 10, e0123777 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 62.

    Dawes, E. J., Zhuang, S., Sinden, R. E. & Basáñez, M.-G. The temporal dynamics of Plasmodium density through the sporogonic cycle within Anopheles mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 103, 1197–1198 (2009).

    PubMed  Google Scholar 

  • 63.

    Churcher, T. S. et al. Probability of transmission of malaria from mosquito to human is regulated by mosquito parasite density in naïve and vaccinated hosts. PLOS Pathog. 13, e1006108 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 64.

    Nacher, M. Does the shape of Plasmodium falciparum gametocytes have a function? Med. Hypotheses 62, 618–619 (2004).

    PubMed  Google Scholar 

  • 65.

    Nixon, C. P. Plasmodium falciparum gametocyte transit through the cutaneous microvasculature: A new target for malaria transmission blocking vaccines? Hum. Vaccines Immunother. 12, 3189–3195 (2016).

    Google Scholar 

  • 66.

    Neveu, G. et al. Plasmodium falciparum gametocyte-infected erythrocytes do not adhere to human primary erythroblasts. Sci. Rep. 8, 1–11 (2018).

    CAS  Google Scholar 

  • 67.

    Barraclough, R. K., Duval, L., Talman, A. M., Ariey, F. & Robert, V. Attraction between sexes: male-female gametocyte behaviour within a Leucocytozoon toddi (Haemosporida). Parasitol. Res. 102, 1321–1327 (2008).

    PubMed  Google Scholar 

  • 68.

    Jovani, R. et al. Double gametocyte infections in apicomplexan parasites of birds and reptiles. Parasitol. Res. 94, 155–157 (2004).

    PubMed  Google Scholar 

  • 69.

    Paul, R. E. L., Bonnet, S., Boudin, C., Tchuinkam, T. & Robert, V. Aggregation in malaria parasites places limits on mosquito infection rates. Infect. Genet. Evol. 7, 577–586 (2007).

    CAS  PubMed  Google Scholar 

  • 70.

    Dekker, T. et al. Selection of biting sites on a human host by Anopheles gambiae s.s., An. arabiensis and An. quadriannulatus. Entomol. Exp. Appl. 87, 295–300 (1998).

    Google Scholar 

  • 71.

    Braack, L. et al. Biting behaviour of African malaria vectors: 1. where do the main vector species bite on the human body. Parasit. Vectors 8, 76 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 72.

    Bompard, A. et al. High Plasmodium infection intensity in naturally infected malaria vectors in Africa. bioRxiv 780064 (2019).

  • 73.

    Valkiunas, G. Avian Malaria Parasites and other Haemosporidia. (CRC Press, 2004). Boca Raton

  • 74.

    Vézilier, J., Nicot, A., Gandon, S. & Rivero, A. Insecticide resistance and malaria transmission: infection rate and oocyst burden in Culex pipiens mosquitoes infected with Plasmodium relictum. Malar. J. 9, 379 (2010).

    PubMed  PubMed Central  Google Scholar 

  • 75.

    Nakagawa, S. & Schielzeth, H. Repeatability for gaussian and non-gaussian data: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 85, 935–956 (2010).

    PubMed  Google Scholar 

  • 76.

    Dongen, S. V. Molenberghs & Matthysen. The statistical analysis of fluctuating asymmetry: REML estimation of a mixed regression model. J. Evol. Biol. 12, 94–102 (1999).

    Google Scholar 

  • 77.

    Verbeke, G. & Molenberghs, G. Linear Mixed Models for Longitudinal Data. (Springer-Verlag, 2000).

  • 78.

    Palmer, A. R. & Strobeck, C. Fluctuating asymmetry: Measurement, analysis, patterns. Annu. Rev. Ecol. Syst. 17, 391–421 (1986).

    Google Scholar 

  • 79.

    Lazić, M. M., Kaliontzopoulou, A., Carretero, M. A. & Crnobrnja-Isailović, J. Lizards from urban areas are more asymmetric: Using fluctuating asymmetry to evaluate environmental disturbance. PLOS ONE 8, e84190 (2013).

    ADS  PubMed  PubMed Central  Google Scholar 

  • 80.

    Barto, N. K. MuMIn: Multi-model inference. (2014).

  • 81.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 067, (2015).

  • 82.

    Crawley, M. J. The R Book. (John Wiley & Sons, 2012). Chichester.

  • 83.

    Bolker, B. M. Ecological Models and Data in R. (Princeton University Press, 2008). Princeton and Oxford.


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