Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies.
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.
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow G12 8QQ, Scotland; Medical Research Council-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, Scotland; Odum School of Ecology, University of Georgia, Athens, GA 30602; daniel.streicker@glasgow.ac.uk.
Daniel G
DG
Streicker
Odum School of Ecology, University of Georgia, Athens, GA 30602; Institute of Vertebrate Biology, Czech Academy of Sciences, 603 65 Brno, Czech Republic; Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, 24306 Ploen, Germany;
Jamie C
JC
Winternitz
Odum School of Ecology, University of Georgia, Athens, GA 30602;
Dara A
DA
Satterfield
Poxvirus and Rabies Branch, Division of High Consequence Pathogen and Pathology, Centers for Disease Control and Prevention, Atlanta, GA 30329;
Rene Edgar
RE
Condori-Condori
Medical Research Council-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, Scotland;
Alice
A
Broos
Association for the Conservation and Development of Natural Resources, Lima-41, Peru;
Carlos
C
Tello
Instituto Nacional de Salud, Ministry of Health of Peru, Lima-11, Peru;
Sergio
S
Recuenco
Poxvirus and Rabies Branch, Division of High Consequence Pathogen and Pathology, Centers for Disease Control and Prevention, Atlanta, GA 30329;
Andrés
A
Velasco-Villa
Odum School of Ecology, University of Georgia, Athens, GA 30602;
Sonia
S
Altizer
Association for the Conservation and Development of Natural Resources, Lima-41, Peru; National Service of Agrarian Health, SENASA-Peru, Lima-12, Peru.
William
W
Valderrama
D000818:Animals; D001499:Bayes Theorem; D005075:Biological Evolution; D002685:Chiroptera / Q000821:virology*; D016679:Genome, Viral; D005843:Geography; D054884:Host-Pathogen Interactions; D040582:Inheritance Patterns / Q000235:genetics; D008297:Male; D018895:Microsatellite Repeats / Q000235:genetics; D010568:Peru / Q000453:epidemiology; D011818:Rabies / Q000453:epidemiology*; D011820:Rabies virus / Q000235:genetics; D012621:Seasons
Desmodus; forecasting; sex bias; spatial dynamics; zoonotic disease