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Multiple introductions of Zika virus into the United States revealed through genomic epidemiology

View ORCID ProfileNathan D Grubaugh, Jason T Ladner, Moritz UG Kraemer, Gytis Dudas, Amanda L Tan, Karthik Gangavarapu, Michael R Wiley, Stephen White, Julien Thézé, Diogo M Magnani, Karla Prieto, Daniel Reyes, Andrea Bingham, Lauren M Paul, Refugio Robles-Sikisaka, Glenn Oliveira, Darryl Pronty, Hayden C Metsky, Mary Lynn Baniecki, Kayla G Barnes, Bridget Chak, Catherine A Freije, Adrianne Gladden-Young, Andreas Gnirke, Cynthia Luo, Bronwyn MacInnis, Christian B Matranga, Daniel J Park, James Qu, Stephen F Schaffner, Christopher Tomkins-Tinch, Kendra L West, Sarah M Winnicki, Shirlee Wohl, Nathan L Yozwiak, Joshua Quick, Joseph R Fauver, Kamran Khan, Shannon E Brent, Robert C Reiner Jr., Paola N Lichtenberger, Michael Ricciardi, Varian K Bailey, David I Watkins, Marshall R Cone, Edgar W Kopp IV, Kelly N Hogan, Andrew C Cannons, Reynald Jean, Robert F Garry, Nicholas J Loman, Nuno R Faria, Mario C Porcelli, Chalmers Vasquez, Elyse R Nagle, Derek AT Cummings, Danielle Stanek, Andrew Rambaut, Mariano Sanchez-Lockhart, Pardis C Sabeti, Leah D Gillis, Scott F Michael, Trevor Bedford, Oliver G Pybus, Sharon Isern, Gustavo Palacios, View ORCID ProfileKristian G Andersen
doi: https://doi.org/10.1101/104794
Nathan D Grubaugh
1Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA 92037, USA
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  • ORCID record for Nathan D Grubaugh
Jason T Ladner
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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Moritz UG Kraemer
3Department of Zoology, University of Oxford, Oxford OX1 3PS, UK
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Gytis Dudas
44Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA
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Amanda L Tan
5Department of Biological Sciences, College of Arts and Sciences, Florida Gulf Coast University, Fort Myers, FL, 33965,USA
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Karthik Gangavarapu
1Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA 92037, USA
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Michael R Wiley
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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Stephen White
6Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Miami, FL, 33125,USA
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Julien Thézé
3Department of Zoology, University of Oxford, Oxford OX1 3PS, UK
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Diogo M Magnani
7Department of Pathology, University of Miami Miller School of Medicine, Miami, FL, 33136, USA
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Karla Prieto
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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Daniel Reyes
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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Andrea Bingham
8Bureau of Epidemiology, Division of Disease Control and Health Protection, Florida Department of Health, Tallahassee, FL, 32399, USA
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Lauren M Paul
5Department of Biological Sciences, College of Arts and Sciences, Florida Gulf Coast University, Fort Myers, FL, 33965,USA
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Refugio Robles-Sikisaka
1Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA 92037, USA
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Glenn Oliveira
9Scripps Translational Science Institute, La Jolla, CA 92037, USA
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Darryl Pronty
6Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Miami, FL, 33125,USA
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Hayden C Metsky
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Mary Lynn Baniecki
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Kayla G Barnes
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Bridget Chak
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Catherine A Freije
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Adrianne Gladden-Young
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Andreas Gnirke
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Cynthia Luo
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Bronwyn MacInnis
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Christian B Matranga
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Daniel J Park
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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James Qu
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Stephen F Schaffner
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Christopher Tomkins-Tinch
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Kendra L West
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Sarah M Winnicki
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Shirlee Wohl
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Nathan L Yozwiak
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Joshua Quick
11Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, UK
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Joseph R Fauver
12Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO 80523, USA
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Kamran Khan
13Li Ka Shing Knowledge Institute, St Michael´s Hospital, Toronto, ON M5B 1T8, Canada
14Division of Infectious Diseases, Department of Medicine, University of Toronto, Toronto, ON M5B 1T8, Canada
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Shannon E Brent
13Li Ka Shing Knowledge Institute, St Michael´s Hospital, Toronto, ON M5B 1T8, Canada
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Robert C Reiner Jr.
15Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA 98121, USA
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Paola N Lichtenberger
16Division of Infectious Diseases, University of Miami Miller School of Medicine, Miami, FL, 33155, USA
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Michael Ricciardi
7Department of Pathology, University of Miami Miller School of Medicine, Miami, FL, 33136, USA
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Varian K Bailey
7Department of Pathology, University of Miami Miller School of Medicine, Miami, FL, 33136, USA
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David I Watkins
7Department of Pathology, University of Miami Miller School of Medicine, Miami, FL, 33136, USA
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Marshall R Cone
17Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Tampa, FL, 33612, USA
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Edgar W Kopp IV
17Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Tampa, FL, 33612, USA
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Kelly N Hogan
17Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Tampa, FL, 33612, USA
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Andrew C Cannons
17Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Tampa, FL, 33612, USA
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Reynald Jean
18Florida Department of Health in Miami-Dade County, Miami, FL, 33125, USA
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Robert F Garry
19Department of Microbiology and Immunology, Tulane University School of Medicine, New Orleans, LA 70112, USA
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Nicholas J Loman
11Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, UK
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Nuno R Faria
3Department of Zoology, University of Oxford, Oxford OX1 3PS, UK
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Mario C Porcelli
20Miami-Dade County Mosquito Control, Miami, FL, 33178 USA
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Chalmers Vasquez
20Miami-Dade County Mosquito Control, Miami, FL, 33178 USA
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Elyse R Nagle
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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Derek AT Cummings
21Department of Biology and Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32610, USA
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Danielle Stanek
8Bureau of Epidemiology, Division of Disease Control and Health Protection, Florida Department of Health, Tallahassee, FL, 32399, USA
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Andrew Rambaut
22Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK
23Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA
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Mariano Sanchez-Lockhart
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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Pardis C Sabeti
10The Broad Institute of MIT and Harvard, Cambridge, MA 02142,USA
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Leah D Gillis
6Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Miami, FL, 33125,USA
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Scott F Michael
5Department of Biological Sciences, College of Arts and Sciences, Florida Gulf Coast University, Fort Myers, FL, 33965,USA
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Trevor Bedford
44Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA
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Oliver G Pybus
3Department of Zoology, University of Oxford, Oxford OX1 3PS, UK
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Sharon Isern
5Department of Biological Sciences, College of Arts and Sciences, Florida Gulf Coast University, Fort Myers, FL, 33965,USA
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Gustavo Palacios
2Center for Genome Sciences,U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702, USA
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  • For correspondence: andersen@scripps.edu gustavo.f.palacios.ctr@mail.mil
Kristian G Andersen
1Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA 92037, USA
9Scripps Translational Science Institute, La Jolla, CA 92037, USA
24Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA 92037, USA
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  • ORCID record for Kristian G Andersen
  • For correspondence: andersen@scripps.edu gustavo.f.palacios.ctr@mail.mil
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Abstract

Zika virus (ZIKV) is causing an unprecedented epidemic linked to severe congenital syndromes1,2. In July 2016, mosquito-borne ZIKV transmission was first reported in the continental United States and since then, hundreds of locally-acquired infections have been reported in Florida3. To gain insights into the timing, source, and likely route(s) of introduction of ZIKV into the continental United States, we tracked the virus from its first detection in Miami, Florida by direct sequencing of ZIKV genomes from infected patients and Aedes aegypti mosquitoes. We show that at least four distinct ZIKV introductions contributed to the outbreak in Florida and that local transmission likely started in the spring of 2016 - several months before its initial detection. By analyzing surveillance and genetic data, we discovered that ZIKV moved among transmission zones in Miami. Our analyses show that most introductions are phylogenetically linked to the Caribbean, a finding corroborated by the high incidence rates and traffic volumes from the region into the Miami area. By comparing mosquito abundance and travel flows, we describe the areas of southern Florida that are especially vulnerable to ZIKV introductions. Our study provides a deeper understanding of how ZIKV initiates and sustains transmission in new regions.

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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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Multiple introductions of Zika virus into the United States revealed through genomic epidemiology
Nathan D Grubaugh, Jason T Ladner, Moritz UG Kraemer, Gytis Dudas, Amanda L Tan, Karthik Gangavarapu, Michael R Wiley, Stephen White, Julien Thézé, Diogo M Magnani, Karla Prieto, Daniel Reyes, Andrea Bingham, Lauren M Paul, Refugio Robles-Sikisaka, Glenn Oliveira, Darryl Pronty, Hayden C Metsky, Mary Lynn Baniecki, Kayla G Barnes, Bridget Chak, Catherine A Freije, Adrianne Gladden-Young, Andreas Gnirke, Cynthia Luo, Bronwyn MacInnis, Christian B Matranga, Daniel J Park, James Qu, Stephen F Schaffner, Christopher Tomkins-Tinch, Kendra L West, Sarah M Winnicki, Shirlee Wohl, Nathan L Yozwiak, Joshua Quick, Joseph R Fauver, Kamran Khan, Shannon E Brent, Robert C Reiner Jr., Paola N Lichtenberger, Michael Ricciardi, Varian K Bailey, David I Watkins, Marshall R Cone, Edgar W Kopp IV, Kelly N Hogan, Andrew C Cannons, Reynald Jean, Robert F Garry, Nicholas J Loman, Nuno R Faria, Mario C Porcelli, Chalmers Vasquez, Elyse R Nagle, Derek AT Cummings, Danielle Stanek, Andrew Rambaut, Mariano Sanchez-Lockhart, Pardis C Sabeti, Leah D Gillis, Scott F Michael, Trevor Bedford, Oliver G Pybus, Sharon Isern, Gustavo Palacios, Kristian G Andersen
bioRxiv 104794; doi: https://doi.org/10.1101/104794
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Multiple introductions of Zika virus into the United States revealed through genomic epidemiology
Nathan D Grubaugh, Jason T Ladner, Moritz UG Kraemer, Gytis Dudas, Amanda L Tan, Karthik Gangavarapu, Michael R Wiley, Stephen White, Julien Thézé, Diogo M Magnani, Karla Prieto, Daniel Reyes, Andrea Bingham, Lauren M Paul, Refugio Robles-Sikisaka, Glenn Oliveira, Darryl Pronty, Hayden C Metsky, Mary Lynn Baniecki, Kayla G Barnes, Bridget Chak, Catherine A Freije, Adrianne Gladden-Young, Andreas Gnirke, Cynthia Luo, Bronwyn MacInnis, Christian B Matranga, Daniel J Park, James Qu, Stephen F Schaffner, Christopher Tomkins-Tinch, Kendra L West, Sarah M Winnicki, Shirlee Wohl, Nathan L Yozwiak, Joshua Quick, Joseph R Fauver, Kamran Khan, Shannon E Brent, Robert C Reiner Jr., Paola N Lichtenberger, Michael Ricciardi, Varian K Bailey, David I Watkins, Marshall R Cone, Edgar W Kopp IV, Kelly N Hogan, Andrew C Cannons, Reynald Jean, Robert F Garry, Nicholas J Loman, Nuno R Faria, Mario C Porcelli, Chalmers Vasquez, Elyse R Nagle, Derek AT Cummings, Danielle Stanek, Andrew Rambaut, Mariano Sanchez-Lockhart, Pardis C Sabeti, Leah D Gillis, Scott F Michael, Trevor Bedford, Oliver G Pybus, Sharon Isern, Gustavo Palacios, Kristian G Andersen
bioRxiv 104794; doi: https://doi.org/10.1101/104794

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