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Identity-by-descent relatedness estimates with uncertainty characterise departure from isolation-by-distance between Plasmodium falciparum populations on the Colombian-Pacific coast

View ORCID ProfileAimee R. Taylor, View ORCID ProfileDiego F. Echeverry, View ORCID ProfileTimothy J. C. Anderson, View ORCID ProfileDaniel E. Neafsey, View ORCID ProfileCaroline O. Buckee
doi: https://doi.org/10.1101/2020.04.10.035303
Aimee R. Taylor
1Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
2Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
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  • For correspondence: ataylor@hsph.harvard.edu
Diego F. Echeverry
3Centro Internacional de Entrenamiento e Investigaciones Médicas (CIDEIM), Cali, Colombia
4Universidad Icesi, Cali, Colombia
5Departamento de Microbiologia, Facultad de Salud, Universidad del Valle, Cali, Colombia
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Timothy J. C. Anderson
6Department of Genetics, Texas Biomedical Research Institute, San Antonio, Texas, USA
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Daniel E. Neafsey
2Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
7Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
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Caroline O. Buckee
1Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
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Abstract

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 to date. 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. The fraction of highly-related sample pairs (whose classification accounts for uncertainty) was greater within cities versus between. However, based on both the fraction of highly-related sample pairs 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 three separate transmission events involving parasites from five different 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 and alternative hypotheses. For the first time in malaria epidemiology, we account for uncertainty around estimated relatedness (an important consideration for future studies that plan to use genotype versus whole genome sequence data to estimate IBD-based relatedness); we also use a threshold-free approach to compare parasite populations, and identify clonal components in a statistically principled manner. The approaches we employ could be adapted to other recombining organisms with mixed mating systems, thus have broad relevance.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/artaylor85/ColombianBarcode

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 10, 2020.
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Identity-by-descent relatedness estimates with uncertainty characterise departure from isolation-by-distance between Plasmodium falciparum populations on the Colombian-Pacific coast
Aimee R. Taylor, Diego F. Echeverry, Timothy J. C. Anderson, Daniel E. Neafsey, Caroline O. Buckee
bioRxiv 2020.04.10.035303; doi: https://doi.org/10.1101/2020.04.10.035303
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Identity-by-descent relatedness estimates with uncertainty characterise departure from isolation-by-distance between Plasmodium falciparum populations on the Colombian-Pacific coast
Aimee R. Taylor, Diego F. Echeverry, Timothy J. C. Anderson, Daniel E. Neafsey, Caroline O. Buckee
bioRxiv 2020.04.10.035303; doi: https://doi.org/10.1101/2020.04.10.035303

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