Genetic relatedness analysis reveals the cotransmission of genetically related Plasmodium falciparum parasites in Thiès, Senegal
Tóm tắt
As public health interventions drive parasite populations to elimination, genetic epidemiology models that incorporate population genomics can be powerful tools for evaluating the effectiveness of continued intervention. However, current genetic epidemiology models may not accurately simulate the population genetic profile of parasite populations, particularly with regard to polygenomic (multi-strain) infections. Current epidemiology models simulate polygenomic infections via superinfection (multiple mosquito bites), despite growing evidence that cotransmission (a single mosquito bite) may contribute to polygenomic infections. Here, we quantified the relatedness of strains within 31 polygenomic infections collected from patients in Thiès, Senegal using a hidden Markov model to measure the proportion of the genome that is inferred to be identical by descent. We found that polygenomic infections can be composed of highly related parasites and that superinfection models drastically underestimate the relatedness of strains within polygenomic infections. Our findings suggest that cotransmission is a major contributor to polygenomic infections in Thiès, Senegal. The incorporation of cotransmission into existing genetic epidemiology models may enhance our ability to characterize and predict changes in population structure associated with reduced transmission intensities and the emergence of important phenotypes like drug resistance that threaten to undermine malaria elimination activities.
Tài liệu tham khảo
Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, et al. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000;17:1467–82.
Obaldia 3rd N, Baro NK, Calzada JE, Santamaria AM, Daniels R, Wong W, et al. Clonal outbreak of Plasmodium falciparum infection in eastern Panama. J Infect Dis. 2015;211:1087–96.
Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, et al. Population genetic correlates of declining transmission in a human pathogen. Mol Ecol. 2013;22:273–85.
Daniels R, Chang H-H, Séne PD, Park DC, Neafsey DE, Schaffner SF, et al. Genetic surveillance detects both clonal and epidemic transmission of malaria following enhanced intervention in Senegal. PLoS One. 2013;8:e60780.
Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci. 2015;112:7067–72.
Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012;487:375–9.
Conway DJ, Greenwood BM, McBride JS. The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology. 1991;103:1–5.
Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, et al. Close kinship within multiple-genotype malaria parasite infections. Proc R Soc London B Biol Sci. 2012;279(1738):2589–98.
Nair S, Nkhoma SC, Serre D, Zimmerman PA, Gorena K, Daniel BJ, et al. Single-cell genomics for dissection of complex malaria infections. Genome Res. 2014;24:1028–38.
Sutton PL, Neyra V, Hernandez JN, Branch OH. Plasmodium falciparum and Plasmodium vivax Infections in the Peruvian Amazon: propagation of complex, multiple allele-type infections without super-infection. Am J Trop Med Hyg. 2009;81:950–60.
Ross R. Some quantitative studies in epidemiology. Nature. 1911;87:466–7.
Alizon S, de Roode JC, Michalakis Y. Multiple infections and the evolution of virulence. Ecol Lett. 2013;16:556–67.
Lion S. Multiple infections, kin selection and the evolutionary epidemiology of parasite traits. J Evol Biol. 2013;26:2107–22.
van Baalen M, Sabelis MW. The dynamics of multiple infection and the evolution of virulence. Am Nat. 1995;146:881–910.
Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8:e1002588.
Trape JF, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, Druilhe P, et al. Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg. 1992;47(2):181–9.
Mouzin E, Thior P, Diouf M, Sambou B. Focus on Senegal roll back malaria: Progress and Impact Series. Geneva: World Health Organization; 2010.
Daniels R, Volkman S, Milner D, Mahesh N, Neafsey D, Park D, et al. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J. 2008;7:223.
Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinforma. 2009;25:1754–60.
Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37:D539–43.
DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43:491–8.
Galinsky K, Valim C, Salmier A, de Thoisy B, Musset L, Legrand E, et al. COIL: a methodology for evaluating malarial complexity of infection using likelihood from single nucleotide polymorphism data. Malar J. 2015;14:4.
Chang H-H, Park DJ, Galinsky KJ, Schaffner SF, Ndiaye D, Ndir O, et al. Genomic sequencing of Plasmodium falciparum malaria parasites from Senegal reveals the demographic history of the population. Mol Biol Evol. 2012;29:3427–39.
Browning SR, Browning BL. Haplotype phasing: existing methods and new developments. Nat Rev Genet. 2011;12:703–14.
Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9:e1001165.
Vaughan AM, Pinapati RS, Cheeseman IH, Camargo N, Fishbaugher M, Checkley LA, et al. Plasmodium falciparum genetic crosses in a humanized mouse model. Nat Methods. 2015;12:631–3.
Chang H-H, Childs LM, Buckee CO. Variation in infection length and superinfection enhance selection efficiency in the human malaria parasite. Sci Rep. 2016;6:26370.
Klein EY, Smith DL, Laxminarayan R, Levin S. Superinfection and the evolution of resistance to antimalarial drugs. Proc R Soc B. 2012;279:3834–42.
Childs LM, Buckee CO. Dissecting the determinants of malaria chronicity: why within-host models struggle to reproduce infection dynamics. J R Soc Interface. 2015;12:20141379. The Royal Society.