Identity-by-descent with uncertainty characterises connectivity of Plasmodium falciparum populations on the Colombian-Pacific coast
Autoři:
Aimee R. Taylor aff001; Diego F. Echeverry aff003; Timothy J. C. Anderson aff006; Daniel E. Neafsey aff002; Caroline O. Buckee aff001
Působiště autorů:
Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
aff001; Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
aff002; Centro Internacional de Entrenamiento e Investigaciones Médicas (CIDEIM), Cali, Colombia
aff003; Universidad Icesi, Calle 18 No. 122-135, Cali, Colombia
aff004; Departamento de Microbiologia, Facultad de Salud, Universidad del Valle, Cali, Colombia
aff005; Disease Intervention and Prevention Program, Texas Biomedical Research Institute, San Antonio, Texas, USA
aff006; Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
aff007
Vyšlo v časopise:
Identity-by-descent with uncertainty characterises connectivity of Plasmodium falciparum populations on the Colombian-Pacific coast. PLoS Genet 16(11): e1009101. doi:10.1371/journal.pgen.1009101
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009101
Souhrn
Characterising connectivity between geographically separated biological populations is a common goal in many fields. Recent approaches to understanding connectivity between malaria parasite populations, with implications for disease control efforts, have used estimates of relatedness based on identity-by-descent (IBD). However, uncertainty around estimated relatedness has not been accounted for. IBD-based relatedness estimates with uncertainty were computed for pairs of monoclonal Plasmodium falciparum samples collected from five cities on the Colombian-Pacific coast where long-term clonal propagation of P. falciparum is frequent. The cities include two official ports, Buenaventura and Tumaco, that are separated geographically but connected by frequent marine traffic. Fractions of highly-related sample pairs (whose classification using a threshold accounts for uncertainty) were greater within cities versus between. However, based on both highly-related fractions and on a threshold-free approach (Wasserstein distances between parasite populations) connectivity between Buenaventura and Tumaco was disproportionally high. Buenaventura-Tumaco connectivity was consistent with transmission events involving parasites from five clonal components (groups of statistically indistinguishable parasites identified under a graph theoretic framework). To conclude, P. falciparum population connectivity on the Colombian-Pacific coast abides by accessibility not isolation-by-distance, potentially implicating marine traffic in malaria transmission with opportunities for targeted intervention. Further investigations are required to test this hypothesis. For the first time in malaria epidemiology (and to our knowledge in ecological and epidemiological studies more generally), we account for uncertainty around estimated relatedness (an important consideration for studies that plan to use genotype versus whole genome sequence data to estimate IBD-based relatedness); we also use threshold-free methods to compare parasite populations and identify clonal components. Threshold-free methods are especially important in analyses of malaria parasites and other recombining organisms with mixed mating systems where thresholds do not have clear interpretation (e.g. due to clonal propagation) and thus undermine the cross-comparison of studies.
Klíčová slova:
Cities – Colombia – DNA recombination – Malaria – Malarial parasites – Parasitic diseases – Plasmodium – Single nucleotide polymorphisms
Zdroje
1. Dalmat R, Naughton B, Kwan-Gett TS, Slyker J, Stuckey EM. Use cases for genetic epidemiology in malaria elimination. Malaria journal. 2019;18(1):163. doi: 10.1186/s12936-019-2784-0
2. Holder M, Lewis PO. Phylogeny estimation: traditional and Bayesian approaches. Nature reviews genetics. 2003;4(4):275–284. doi: 10.1038/nrg1044
3. Biek R, Pybus OG, Lloyd-Smith JO, Didelot X. Measurably evolving pathogens in the genomic era. Trends in ecology & evolution. 2015;30(6):306–313. doi: 10.1016/j.tree.2015.03.009
4. Thompson EA. Identity by descent: variation in meiosis, across genomes, and in populations. Genetics. 2013;194(2):301–326. doi: 10.1534/genetics.112.148825
5. Taylor AR, Schaffner SF, Cerqueira GC, Nkhoma SC, Anderson TJ, Sriprawat K, et al. Quantifying connectivity between local Plasmodium falciparum malaria parasite populations using identity by descent. PLoS genetics. 2017;13(10):e1007065. doi: 10.1371/journal.pgen.1007065 29077712
6. Grant AG, Kalisz S. Do selfing species have greater niche breadth? Support from ecological niche modeling. Evolution. 2020;74(1):73–88. doi: 10.1111/evo.13870
7. Mattila TM, Laenen B, Slotte T. Population genomics of transitions to selfing in Brassicaceae model systems. In: Statistical Population Genomics. Springer; 2020. p. 269–287.
8. Siegel SV, Rayner JC. Single cell sequencing shines a light on malaria parasite relatedness in complex infections. Trends in Parasitology. 2020;36(2):83–85. doi: 10.1016/j.pt.2019.12.007
9. Macdonald G, et al. The analysis of infection rates in diseases in which super infection occurs. Tropical diseases bulletin. 1950;47:907–915. 14798656
10. Nåsell I. On superinfection in malaria. Mathematical Medicine and Biology: A Journal of the IMA. 1986;3(3):211–227. doi: 10.1093/imammb/3.3.211
11. Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, et al. Close kinship within multiple-genotype malaria parasite infections. Proceedings of the Royal Society B: Biological Sciences. 2012;279(1738):2589–2598. doi: 10.1098/rspb.2012.0113 22398165
12. Nkhoma SC, Trevino SG, Gorena KM, Nair S, Khoswe S, Jett C, et al. Co-transmission of Related Malaria Parasite Lineages Shapes Within-Host Parasite Diversity. Cell Host & Microbe. 2020;27(1):93–103. doi: 10.1016/j.chom.2019.12.001 31901523
13. Echeverry DF, Nair S, Osorio L, Menon S, Murillo C, Anderson TJ. Long term persistence of clonal malaria parasite Plasmodium falciparum lineages in the Colombian Pacific region. BMC genetics. 2013;14(1):2. doi: 10.1186/1471-2156-14-2
14. Omedo I, Mogeni P, Rockett K, Kamau A, Hubbart C, Jeffreys A, et al. Geographic-genetic analysis of Plasmodium falciparum parasite populations from surveys of primary school children in Western Kenya. Wellcome open research. 2017;2:29. doi: 10.12688/wellcomeopenres.11228.2 28944299
15. Omedo I, Mogeni P, Bousema T, Rockett K, Amambua-Ngwa A, Oyier I, et al. Micro-epidemiological structuring of Plasmodium falciparum parasite populations in regions with varying transmission intensities in Africa. Wellcome open research. 2017;2:10. doi: 10.12688/wellcomeopenres.10784.1
16. Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri AR, et al. Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa. Elife. 2019;8:e43510. doi: 10.7554/eLife.43510
17. Rodríguez JCP, Uribe GÁ, Araújo RM, Narváez PC, Valencia SH. Epidemiology and control of malaria in Colombia. Memórias do Instituto Oswaldo Cruz. 2011;106:114–122. doi: 10.1590/S0074-02762011000900015
18. Feged-Rivadeneira A, Ángel A, González-Casabianca F, Rivera C. Malaria intensity in Colombia by regions and populations. PloS One. 2018;13(9). doi: 10.1371/journal.pone.0203673 30208075
19. Castellanos A, Chaparro-Narváez P, Morales-Plaza CD, Alzate A, Padilla J, Arévalo M, et al. Malaria in gold-mining areas in Colombia. Memorias do Instituto Oswaldo Cruz. 2016;111(1):59–66. doi: 10.1590/0074-02760150382 26814645
20. Recht J, Siqueira AM, Monteiro WM, Herrera SM, Herrera S, Lacerda MV. Malaria in Brazil, Colombia, Peru and Venezuela: current challenges in malaria control and elimination. Malaria journal. 2017;16(1):273. doi: 10.1186/s12936-017-1925-6
21. Daniels JP. Increasing malaria in Venezuela threatens regional progress. The Lancet Infectious Diseases. 2018;18(3):257. doi: 10.1016/S1473-3099(18)30086-0
22. Knudson A, González-Casabianca F, Feged-Rivadeneira A, Pedreros MF, Aponte S, Olaya A, et al. Spatio-temporal dynamics of Plasmodium falciparum transmission within a spatial unit on the Colombian Pacific Coast. Scientific Reports. 2020;10(1):1–16. doi: 10.1038/s41598-020-60676-1 32111872
23. Grillet ME, Villegas L, Oletta JF, Tami A, Conn JE. Malaria in Venezuela requires response. Science. 2018;359(6375):528–528.
24. Jaramillo-Ochoa R, Sippy R, Farrell DF, Cueva-Aponte C, Beltrán-Ayala E, Gonzaga JL, et al. Effects of political instability in Venezuela on malaria resurgence at Ecuador–Peru border, 2018. Emerging infectious diseases. 2019;25(4):834. doi: 10.3201/eid2504.181355 30698522
25. Daniels JP. Venezuela in crisis. The Lancet Infectious Diseases. 2019;19(1):28. doi: 10.1016/S1473-3099(18)30745-X
26. Rodríguez-Morales AJ, Suárez JA, Risquez A, Villamil-Gómez WE, Paniz-Mondolfi A. Consequences of Venezuela’s massive migration crisis on imported malaria in Colombia, 2016-2018. Travel Medicine and Infectious Disease. 2019;28:98–99. doi: 10.1016/j.tmaid.2019.02.004
27. Parker DM, Landier J, Thu AM, Lwin KM, Delmas G, Nosten FH, et al. Scale up of a Plasmodium falciparum elimination program and surveillance system in Kayin State, Myanmar. Wellcome open research. 2017;2. doi: 10.12688/wellcomeopenres.12741.2 29384151
28. Landier J, Parker DM, Thu AM, Lwin KM, Delmas G, Nosten FH, et al. Effect of generalised access to early diagnosis and treatment and targeted mass drug administration on Plasmodium falciparum malaria in Eastern Myanmar: an observational study of a regional elimination programme. The Lancet. 2018;391(10133):1916–1926. doi: 10.1016/S0140-6736(18)30792-X 29703425
29. Blanton RE. Population genetics and molecular epidemiology of eukaryotes. Microbiology spectrum. 2018;6(6). doi: 10.1128/microbiolspec.AME-0002-2018 30387414
30. Wesolowski A, Taylor AR, Chang HH, Verity R, Tessema S, Bailey JA, et al. Mapping malaria by combining parasite genomic and epidemiologic data. BMC medicine. 2018;16(1):1–8. doi: 10.1186/s12916-018-1232-2
31. Gao B, Saralamba S, Lubell Y, White LJ, Dondorp AM, Aguas R. Determinants of MDA impact and designing MDAs towards malaria elimination. Elife. 2020;9:e51773. doi: 10.7554/eLife.51773
32. Taylor AR, Jacob PE, Neafsey DE, Buckee CO. Estimating relatedness between malaria parasites. Genetics. 2019;212(4):1337–1351. doi: 10.1534/genetics.119.302120
33. Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA, et al. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome biology. 2008;9(12):R171. doi: 10.1186/gb-2008-9-12-r171 19077304
34. Peyré G, Cuturi M, et al. Computational optimal transport. Foundations and Trends® in Machine Learning. 2019;11(5-6):355–607. doi: 10.1561/2200000073
35. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–959.
36. Watson JA, Taylor AR, Ashley EA, Dondorp AM, Buckee CO, White NJ, et al. Pre-print: A cautionary note on the use of machine learning algorithms to characterise malaria parasite population structure from genetic distance matrices. bioRxiv. 2020; p. 1–18.
37. Wille M, Holmes EC. The Ecology and Evolution of Influenza Viruses. Cold Spring Harbor Perspectives in Medicine. 2019; p. a038489.
38. Katz EM, Esona MD, Betrapally NS, Lucia A, Neira YR, Rey GJ, et al. Whole-gene analysis of inter-genogroup reassortant rotaviruses from the Dominican Republic: Emergence of equine-like G3 strains and evidence of their reassortment with locally-circulating strains. Virology. 2019;534:114–131. doi: 10.1016/j.virol.2019.06.007 31228725
39. Caugant DA, Brynildsrud OB. Neisseria meningitidis: using genomics to understand diversity, evolution and pathogenesis. Nature Reviews Microbiology. 2019; p. 1–13.
40. Smith JM, Feil EJ, Smith NH. Population structure and evolutionary dynamics of pathogenic bacteria. Bioessays. 2000;22(12):1115–1122. doi: 10.1002/1521-1878(200012)22:12%3C1115::AID-BIES9%3E3.0.CO;2-R
41. Tibayrenc M, Ayala FJ. The clonal theory of parasitic protozoa: 12 years on. Trends in parasitology. 2002;18(9):405–410. doi: 10.1016/S1471-4922(02)02357-7
42. Rajendran C, Su C, Dubey JP. Molecular genotyping of Toxoplasma gondii from Central and South America revealed high diversity within and between populations. Infection, Genetics and Evolution. 2012;12(2):359–368. doi: 10.1016/j.meegid.2011.12.010
43. Nader JL, Mathers TC, Ward BJ, Pachebat JA, Swain MT, Robinson G, et al. Evolutionary genomics of anthroponosis in Cryptosporidium. Nature microbiology. 2019;4(5):826–836. doi: 10.1038/s41564-019-0377-x 30833731
44. Nieuwenhuis BP, James TY. The frequency of sex in fungi. Philosophical Transactions of the Royal Society B: Biological Sciences. 2016;371(1706):20150540. doi: 10.1098/rstb.2015.0540
45. Fruchterman TM, Reingold EM. Graph drawing by force-directed placement. Software: Practice and experience. 1991;21(11):1129–1164.
46. Sáenz FE, Morton LC, Okoth SA, Valenzuela G, Vera-Arias CA, Vélez-Álvarez E, et al. Clonal population expansion in an outbreak of Plasmodium falciparum on the northwest coast of Ecuador. Malaria journal. 2015;14(1):497. doi: 10.1186/s12936-015-1019-2
47. Vera-Arias CA, Castro LE, Gómez-Obando J, Sáenz FE. Diverse origin of Plasmodium falciparum in northwest Ecuador. Malaria journal. 2019;18(1):251. doi: 10.1186/s12936-019-2891-y
48. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164(4):1567–1587.
49. Huestis DL, Dao A, Diallo M, Sanogo ZL, Samake D, Yaro AS, et al. Windborne long-distance migration of malaria mosquitoes in the Sahel. Nature. 2019;574(7778):404–408. doi: 10.1038/s41586-019-1622-4 31578527
50. Verdonschot PF, Besse-Lototskaya AA. Flight distance of mosquitoes (Culicidae): a metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica-Ecology and Management of Inland Waters. 2014;45:69–79. doi: 10.1016/j.limno.2013.11.002
51. Pacheco MA, Schneider KA, Céspedes N, Herrera S, Arévalo-Herrera M, Escalante AA. Limited differentiation among Plasmodium vivax populations from the northwest and to the south Pacific Coast of Colombia: A malaria corridor? PLoS neglected tropical diseases. 2019;13(3):e0007310. doi: 10.1371/journal.pntd.0007310
52. Guagliardo SA, Morrison AC, Barboza JL, Requena E, Astete H, Vazquez-Prokopec G, et al. River boats contribute to the regional spread of the dengue vector Aedes aegypti in the Peruvian Amazon. PLoS neglected tropical diseases. 2015;9(4):e0003648. doi: 10.1371/journal.pntd.0003648 25860352
53. Lounibos LP. Invasions by insect vectors of human disease. Annual review of entomology. 2002;47(1):233–266. doi: 10.1146/annurev.ento.47.091201.145206
54. Montoya-Lerma J, Solarte YA, Giraldo-Calderón GI, Quiñones ML, Ruiz-López F, Wilkerson RC, et al. Malaria vector species in Colombia: a review. Memórias do Instituto Oswaldo Cruz. 2011;106:223–238. doi: 10.1590/S0074-02762011000900028 21881778
55. Gutiérrez LA, Naranjo NJ, Cienfuegos AV, Muskus CE, Luckhart S, Conn JE, et al. Population structure analyses and demographic history of the malaria vector Anopheles albimanus from the Caribbean and the Pacific regions of Colombia. Malaria journal. 2009;8(1):259. doi: 10.1186/1475-2875-8-259 19922672
56. Instituto Nacional de Salud Colombia, Dirección de Vigilancia y Analisis del Riesgo en Salud Pública. Boletín Epidemiológico Semanal: semana epidemiológica 52; 2017. Available from: https://www.ins.gov.co/buscador-eventos/Paginas/Vista-Boletin-Epidemilogico.aspx.
57. Instituto Nacional de Salud Colombia, Dirección de Vigilancia y Analisis del Riesgo en Salud Pública. Boletín Epidemiológico Semanal: semana epidemiológica 52; 2018. Available from: https://www.ins.gov.co/buscador-eventos/Paginas/Vista-Boletin-Epidemilogico.aspx.
58. Instituto Nacional de Salud Colombia, Dirección de Vigilancia y Analisis del Riesgo en Salud Pública. Boletín Epidemiológico Semanal: semana epidemiológica 52; 2019. Available from: https://www.ins.gov.co/buscador-eventos/Paginas/Vista-Boletin-Epidemilogico.aspx.
59. Wabgou M, Vargas D, Carabalí JA. Las migraciones internacionales en Colombia. Investigación & Desarrollo. 2012;20(1):142–167.
60. Ahumada ML, Orjuela LI, Pareja PX, Conde M, Cabarcas DM, Cubillos EFG, et al. Spatial distributions of Anopheles species in relation to malaria incidence at 70 localities in the highly endemic Northwest and South Pacific coast regions of Colombia. Malaria Journal. 2016;15(407):1–16. 27515166
61. Shetty AC, Jacob CG, Huang F, Li Y, Agrawal S, Saunders DL, et al. Genomic structure and diversity of Plasmodium falciparum in Southeast Asia reveal recent parasite migration patterns. Nature communications. 2019;10(1):2665. doi: 10.1038/s41467-019-10121-3 31209259
62. Naranjo-Díaz N, Altamiranda M, Luckhart S, Conn JE, Correa MM. Malaria vectors in ecologically heterogeneous localities of the Colombian Pacific region. PLoS One. 2014;9(8):e103769. doi: 10.1371/journal.pone.0103769
63. Csardi G, Nepusz T. The igraph software package for complex network research. InterJournal, complex systems. 2006;1695(5):1–9.
64. R Core Team. R: A Language and Environment for Statistical Computing; 2018. Available from: https://www.R-project.org/.
65. Schuhmacher D, Bähre B, Gottschlich C, Hartmann V, Heinemann F, Schmitzer B. transport: Computation of Optimal Transport Plans and Wasserstein Distances; 2019. Available from: https://cran.r-project.org/package=transport.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 11
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- Stability of SARS-CoV-2 phylogenies
- Formal commentary
- No association between SCN9A and monogenic human epilepsy disorders
- Oxidative stress antagonizes fluoroquinolone drug sensitivity via the SoxR-SUF Fe-S cluster homeostatic axis