Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague

Amy J Vogler; Voahangy Andrianaivoarimanana; Sandra Telfer; Carina M Hall; Jason W Sahl; Crystal M Hepp; Heather Centner; Genevieve Andersen; Dawn N Birdsell; Lila Rahalison; Roxanne Nottingham; Paul Keim; David M Wagner; Minoarisoa Rajerison

doi:10.1371/journal.pntd.0005887

Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague

Amy J Vogler, Voahangy Andrianaivoarimanana, Sandra Telfer, Carina M Hall, Jason W Sahl, Crystal M Hepp, Heather Centner, Genevieve Andersen, Dawn N Birdsell, Lila Rahalison, Roxanne Nottingham, Paul Keim, David M Wagner, Minoarisoa Rajerison

Aberdeen Centre For Environmental Sustainability

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Abstract

BACKGROUND: Yersinia pestis appears to be maintained in multiple, geographically separate, and phylogenetically distinct subpopulations within the highlands of Madagascar. However, the dynamics of these locally differentiated subpopulations through time are mostly unknown. To address that gap and further inform our understanding of plague epidemiology, we investigated the phylogeography of Y. pestis in Madagascar over an 18 year period.

METHODOLOGY/PRINCIPAL FINDINGS: We generated whole genome sequences for 31 strains and discovered new SNPs that we used in conjunction with previously identified SNPs and variable-number tandem repeats (VNTRs) to genotype 773 Malagasy Y. pestis samples from 1995 to 2012. We mapped the locations where samples were obtained on a fine geographic scale to examine phylogeographic patterns through time. We identified 18 geographically separate and phylogenetically distinct subpopulations that display spatial and temporal stability, persisting in the same locations over a period of almost two decades. We found that geographic areas with higher levels of topographical relief are associated with greater levels of phylogenetic diversity and that sampling frequency can vary considerably among subpopulations and from year to year. We also found evidence of various Y. pestis dispersal events, including over long distances, but no evidence that any dispersal events resulted in successful establishment of a transferred genotype in a new location during the examined time period.

CONCLUSIONS/SIGNIFICANCE: Our analysis suggests that persistent endemic cycles of Y. pestis transmission within local areas are responsible for the long term maintenance of plague in Madagascar, rather than repeated episodes of wide scale epidemic spread. Landscape likely plays a role in maintaining Y. pestis subpopulations in Madagascar, with increased topographical relief associated with increased levels of localized differentiation. Local ecological factors likely affect the dynamics of individual subpopulations and the associated likelihood of observing human plague cases in a given year in a particular location.

Original language	English
Article number	e0005887
Journal	PLoS Neglected Tropical Diseases
Volume	11
Issue number	9
Early online date	5 Sept 2017
DOIs	https://doi.org/10.1371/journal.pntd.0005887
Publication status	Published - 2017

Bibliographical note

Data Availability: All relevant data are within the paper and its Supporting Information files except for the sequence read archives for 31 newly sequenced strains that are available at NCBI under the accession numbers: SRR4175414-SRR4175444. The direct link to this data is: https://www.ncbi.nlm.nih.gov/sra/?term=SRP086709.

Funding: Funding for this study was provided by the US Department of Homeland Security’s Science and Technology Directorate award number HSHQDC-10-C-00139 to PK; the Cowden Endowment at Northern Arizona University; and Wellcome fellowships 081705 and 095171 to ST. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Keywords

Journal Article

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10.1371/journal.pntd.0005887Licence: Other

Temporal phylogeography of Yersinia pestis in Madagascar Insights into the long-term maintenance of plague
Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. https://creativecommons.org/publicdomain/zero/1.0/
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Sandra Telfer
- Biological Sciences, Aberdeen Centre For Environmental Sustainability - Reader
Person: Academic

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Vogler, A. J., Andrianaivoarimanana, V., Telfer, S., Hall, C. M., Sahl, J. W., Hepp, C. M., Centner, H., Andersen, G., Birdsell, D. N., Rahalison, L., Nottingham, R., Keim, P., Wagner, D. M., & Rajerison, M. (2017). Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague. PLoS Neglected Tropical Diseases, 11(9), Article e0005887. https://doi.org/10.1371/journal.pntd.0005887

Vogler, AJ, Andrianaivoarimanana, V, Telfer, S, Hall, CM, Sahl, JW, Hepp, CM, Centner, H, Andersen, G, Birdsell, DN, Rahalison, L, Nottingham, R, Keim, P, Wagner, DM & Rajerison, M 2017, 'Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague', PLoS Neglected Tropical Diseases, vol. 11, no. 9, e0005887. https://doi.org/10.1371/journal.pntd.0005887

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note = "Data Availability: All relevant data are within the paper and its Supporting Information files except for the sequence read archives for 31 newly sequenced strains that are available at NCBI under the accession numbers: SRR4175414-SRR4175444. The direct link to this data is: https://www.ncbi.nlm.nih.gov/sra/?term=SRP086709. Funding: Funding for this study was provided by the US Department of Homeland Security{\textquoteright}s Science and Technology Directorate award number HSHQDC-10-C-00139 to PK; the Cowden Endowment at Northern Arizona University; and Wellcome fellowships 081705 and 095171 to ST. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.",

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AU - Vogler, Amy J

AU - Andrianaivoarimanana, Voahangy

AU - Telfer, Sandra

AU - Hall, Carina M

AU - Sahl, Jason W

AU - Hepp, Crystal M

AU - Centner, Heather

AU - Andersen, Genevieve

AU - Birdsell, Dawn N

AU - Rahalison, Lila

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AU - Keim, Paul

AU - Wagner, David M

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AB - BACKGROUND: Yersinia pestis appears to be maintained in multiple, geographically separate, and phylogenetically distinct subpopulations within the highlands of Madagascar. However, the dynamics of these locally differentiated subpopulations through time are mostly unknown. To address that gap and further inform our understanding of plague epidemiology, we investigated the phylogeography of Y. pestis in Madagascar over an 18 year period.METHODOLOGY/PRINCIPAL FINDINGS: We generated whole genome sequences for 31 strains and discovered new SNPs that we used in conjunction with previously identified SNPs and variable-number tandem repeats (VNTRs) to genotype 773 Malagasy Y. pestis samples from 1995 to 2012. We mapped the locations where samples were obtained on a fine geographic scale to examine phylogeographic patterns through time. We identified 18 geographically separate and phylogenetically distinct subpopulations that display spatial and temporal stability, persisting in the same locations over a period of almost two decades. We found that geographic areas with higher levels of topographical relief are associated with greater levels of phylogenetic diversity and that sampling frequency can vary considerably among subpopulations and from year to year. We also found evidence of various Y. pestis dispersal events, including over long distances, but no evidence that any dispersal events resulted in successful establishment of a transferred genotype in a new location during the examined time period.CONCLUSIONS/SIGNIFICANCE: Our analysis suggests that persistent endemic cycles of Y. pestis transmission within local areas are responsible for the long term maintenance of plague in Madagascar, rather than repeated episodes of wide scale epidemic spread. Landscape likely plays a role in maintaining Y. pestis subpopulations in Madagascar, with increased topographical relief associated with increased levels of localized differentiation. Local ecological factors likely affect the dynamics of individual subpopulations and the associated likelihood of observing human plague cases in a given year in a particular location.

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Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague

Abstract

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Sandra Telfer

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