Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies

Daniel G. Streickera; Jamie C. Winternitzc; Dara A. Satterfield; Rene Edgar Condori-Condori; Alice Broos; Carlos Tello; Sergio Recuenco; Andrés Velasco-Villa; Sonia Altizer; William Valderrama

doi:10.1073/pnas.1606587113

Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies

Daniel G. Streickera, Jamie C. Winternitzc, Dara A. Satterfield, Rene Edgar Condori-Condori, Alice Broos, Carlos Tello, Sergio Recuenco, Andrés Velasco-Villa, Sonia Altizer, William Valderrama

Research output: Contribution to journal › Article › peer-review

90 Scopus citations

Abstract

Anticipating how epidemics will spread across landscapes requires understanding host dispersal events that are notoriously difficult to measure. Here, we contrast host and virus genetic signatures to resolve the spatiotemporal dynamics underlying geographic expansions of vampire bat rabies virus (VBRV) in Peru. Phylogenetic analysis revealed recent viral spread between populations that, according to extreme geographic structure in maternally inherited host mitochondrial DNA, appeared completely isolated. In contrast, greater population connectivity in biparentally inherited nuclear microsatellites explained the historical limits of invasions, suggesting that dispersing male bats spread VBRV between genetically isolated female populations. Host nuclear DNA further indicated unanticipated gene flow through the Andes mountains connecting the VBRV-free Pacific coast to the VBRV-endemic Amazon rainforest. By combining Bayesian phylogeography with landscape resistance models, we projected invasion routes through northern Peru that were validated by real-time livestock rabies mortality data. The first outbreaks of VBRV on the Pacific coast of South America could occur by June 2020, which would have serious implications for agriculture, wildlife conservation, and human health. Our results show that combining host and pathogen genetic data can identify sex biases in pathogen spatial spread, which may be a widespread but underappreciated phenomenon, and demonstrate that genetic forecasting can aid preparedness for impending viral invasions.

Original language	English
Pages (from-to)	10926-10931
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	113
Issue number	39
DOIs	https://doi.org/10.1073/pnas.1606587113
State	Published - 27 Sep 2016

Bibliographical note

Funding Information:
We thank Heather Danaceau, Jennifer Towner, and Victoria Estacio for laboratory assistance and Roman Biek, Barbara Mable, and Mafalda Viana for comments on the manuscript. SENASA contributed surveillance data and livestock samples under an International Cooperative Agreement with the University of Georgia (30-11-2012). The Peruvian Government authorized collection, exportation, and use of genetic resources (RD-222-2009-AG-DGFFS-DGEFFS, 003851-AG-DGFFS, RD-273-2012-AG-DGFFS-DGEFFS, and RD-054-2016-SERFOR-DGGSPFFS). The University of Georgia Advanced Computing Resource Center provided computational resources. Funding was provided by National Science Foundation Grant DEB-1020966 (to D.G.S. and S.A.) and the Pan American Health Organization (W.V.). D.S. was funded by a Sir Henry Dale Fellowship, jointly funded by Wellcome Trust and Royal Society Grant 102507/Z/13/Z. The findings and the conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Keywords

Desmodus
Forecasting
Sex bias
Spatia dynamics
Zoonotic disease

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10.1073/pnas.1606587113

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Streickera, D. G., Winternitzc, J. C., Satterfield, D. A., Condori-Condori, R. E., Broos, A., Tello, C., Recuenco, S., Velasco-Villa, A., Altizer, S., & Valderrama, W. (2016). Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies. Proceedings of the National Academy of Sciences of the United States of America, 113(39), 10926-10931. https://doi.org/10.1073/pnas.1606587113

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abstract = "Anticipating how epidemics will spread across landscapes requires understanding host dispersal events that are notoriously difficult to measure. Here, we contrast host and virus genetic signatures to resolve the spatiotemporal dynamics underlying geographic expansions of vampire bat rabies virus (VBRV) in Peru. Phylogenetic analysis revealed recent viral spread between populations that, according to extreme geographic structure in maternally inherited host mitochondrial DNA, appeared completely isolated. In contrast, greater population connectivity in biparentally inherited nuclear microsatellites explained the historical limits of invasions, suggesting that dispersing male bats spread VBRV between genetically isolated female populations. Host nuclear DNA further indicated unanticipated gene flow through the Andes mountains connecting the VBRV-free Pacific coast to the VBRV-endemic Amazon rainforest. By combining Bayesian phylogeography with landscape resistance models, we projected invasion routes through northern Peru that were validated by real-time livestock rabies mortality data. The first outbreaks of VBRV on the Pacific coast of South America could occur by June 2020, which would have serious implications for agriculture, wildlife conservation, and human health. Our results show that combining host and pathogen genetic data can identify sex biases in pathogen spatial spread, which may be a widespread but underappreciated phenomenon, and demonstrate that genetic forecasting can aid preparedness for impending viral invasions.",

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author = "Streickera, {Daniel G.} and Winternitzc, {Jamie C.} and Satterfield, {Dara A.} and Condori-Condori, {Rene Edgar} and Alice Broos and Carlos Tello and Sergio Recuenco and Andr{\'e}s Velasco-Villa and Sonia Altizer and William Valderrama",

note = "Funding Information: We thank Heather Danaceau, Jennifer Towner, and Victoria Estacio for laboratory assistance and Roman Biek, Barbara Mable, and Mafalda Viana for comments on the manuscript. SENASA contributed surveillance data and livestock samples under an International Cooperative Agreement with the University of Georgia (30-11-2012). The Peruvian Government authorized collection, exportation, and use of genetic resources (RD-222-2009-AG-DGFFS-DGEFFS, 003851-AG-DGFFS, RD-273-2012-AG-DGFFS-DGEFFS, and RD-054-2016-SERFOR-DGGSPFFS). The University of Georgia Advanced Computing Resource Center provided computational resources. Funding was provided by National Science Foundation Grant DEB-1020966 (to D.G.S. and S.A.) and the Pan American Health Organization (W.V.). D.S. was funded by a Sir Henry Dale Fellowship, jointly funded by Wellcome Trust and Royal Society Grant 102507/Z/13/Z. The findings and the conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.",

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Streickera, DG, Winternitzc, JC, Satterfield, DA, Condori-Condori, RE, Broos, A, Tello, C, Recuenco, S, Velasco-Villa, A, Altizer, S & Valderrama, W 2016, 'Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 39, pp. 10926-10931. https://doi.org/10.1073/pnas.1606587113

Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies. / Streickera, Daniel G.; Winternitzc, Jamie C.; Satterfield, Dara A. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 39, 27.09.2016, p. 10926-10931.

Research output: Contribution to journal › Article › peer-review

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AU - Winternitzc, Jamie C.

AU - Satterfield, Dara A.

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AU - Broos, Alice

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AU - Recuenco, Sergio

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Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies

Abstract

Bibliographical note

Keywords

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