Climate and land-use shape the spread of zoonotic yellow fever virus
Sarah C Hill
(1, 2)
,
Simon Dellicour
(3, 4)
,
Ingra M Claro
(5, 6)
,
Patricia C Sequeira
(7)
,
Talita Adelino
(8)
,
Julien Thézé
(9, 2)
,
Chieh-Hsi Wu
(10, 11)
,
Filipe Romero Rebello Moreira
,
Marta Giovanetti
(12, 13)
,
Sabrina L Li
(14, 15)
,
Jaqueline G de Jesus
(5)
,
Felipe J Colón-González
(16)
,
Heather R Chamberlain
,
Oliver Pannell
,
Natalia Tejedor-Garavito
,
Fernanda de Bruycker-Nogueira
,
Allison A Fabri
(7)
,
Maria Angélica Mares-Guia
,
Joilson Xavier
(17)
,
Alexander E Zarebski
,
Arran Hamlet
(18)
,
Maria Anice Mureb Sallum
,
Antonio C da Costa
(19)
,
Erika R Manuli
,
Anna S Levin
,
Luís Filipe Mucci
,
Rosa Maria Tubaki
,
Regiane Maria Tironi de Menezes
,
Juliana Telles de Deus
,
Roberta Spinola
,
Leila Saad
,
Esper G Kallas
,
G.R. William Wint
(20)
,
Pedro S Peixoto
,
Andreza Aruska de Souza Santos
,
Jane P Messina
,
Oliver J Brady
,
Andrew J Tatem
(5)
,
Marc A Suchard
,
Jairo A Mendez-Rico
(5)
,
André Abreu
(5)
,
Renato Santana Aguiar
,
Oliver G Pybus
(5)
,
Guy Baele
(5)
,
Philippe Lemey
(5)
,
Felipe Iani
(5)
,
Mariana S Cunha
(5)
,
Ana M Bispo de Filippis
(5)
,
Ester C Sabino
(5)
,
Nuno R Faria
(5)
1
Royal Veterinary College [London]
2 Department of Zoology
3 SpELL - Spatial Epidemiology Lab
4 Rega Institute for Medical Research [Leuven]
5 FMUSP - Faculdade de Medicina da Universidade de São Paulo
6 The Abdul Latif Jameel Institute for Disease and Emergency Analytics
7 FIOCRUZ - Fundação Oswaldo Cruz / Oswaldo Cruz Foundation
8 FUNED - Fundação Ezequiel Dias
9 UMR EPIA - Unité Mixte de Recherche d'Épidémiologie des maladies Animales et zoonotiques
10 School of Mathematics [Southampton]
11 Institute for Life Sciences
12 Laboratório de Biologia Molecular de Flavivírus [Rio de Janeiro]
13 UFMG - Universidade Federal de Minas Gerais = Federal University of Minas Gerais [Belo Horizonte, Brazil]
14 SoGE - School of Geography and the Environment [Oxford]
15 School of Geography [Nottingham]
16 Department of Infectious Disease Epidemiology, Faculty of Epidemiology and Population
17 ICB - Instituto de Ciências Biológicas [Goiânia, Brésil]
18 Imperial College London
19 UCCS - Unité de Catalyse et Chimie du Solide - UMR 8181
20 Department of Zoology [Oxford]
2 Department of Zoology
3 SpELL - Spatial Epidemiology Lab
4 Rega Institute for Medical Research [Leuven]
5 FMUSP - Faculdade de Medicina da Universidade de São Paulo
6 The Abdul Latif Jameel Institute for Disease and Emergency Analytics
7 FIOCRUZ - Fundação Oswaldo Cruz / Oswaldo Cruz Foundation
8 FUNED - Fundação Ezequiel Dias
9 UMR EPIA - Unité Mixte de Recherche d'Épidémiologie des maladies Animales et zoonotiques
10 School of Mathematics [Southampton]
11 Institute for Life Sciences
12 Laboratório de Biologia Molecular de Flavivírus [Rio de Janeiro]
13 UFMG - Universidade Federal de Minas Gerais = Federal University of Minas Gerais [Belo Horizonte, Brazil]
14 SoGE - School of Geography and the Environment [Oxford]
15 School of Geography [Nottingham]
16 Department of Infectious Disease Epidemiology, Faculty of Epidemiology and Population
17 ICB - Instituto de Ciências Biológicas [Goiânia, Brésil]
18 Imperial College London
19 UCCS - Unité de Catalyse et Chimie du Solide - UMR 8181
20 Department of Zoology [Oxford]
Julien Thézé
- Fonction : Auteur
- PersonId : 184978
- IdHAL : julien-theze
- ORCID : 0000-0001-8188-9494
Filipe Romero Rebello Moreira
- Fonction : Auteur
Heather R Chamberlain
- Fonction : Auteur
Oliver Pannell
- Fonction : Auteur
Natalia Tejedor-Garavito
- Fonction : Auteur
Fernanda de Bruycker-Nogueira
- Fonction : Auteur
Maria Angélica Mares-Guia
- Fonction : Auteur
Alexander E Zarebski
- Fonction : Auteur
Maria Anice Mureb Sallum
- Fonction : Auteur
Erika R Manuli
- Fonction : Auteur
Anna S Levin
- Fonction : Auteur
Luís Filipe Mucci
- Fonction : Auteur
Rosa Maria Tubaki
- Fonction : Auteur
Regiane Maria Tironi de Menezes
- Fonction : Auteur
Juliana Telles de Deus
- Fonction : Auteur
Roberta Spinola
- Fonction : Auteur
Leila Saad
- Fonction : Auteur
Esper G Kallas
- Fonction : Auteur
Pedro S Peixoto
- Fonction : Auteur
Andreza Aruska de Souza Santos
- Fonction : Auteur
Jane P Messina
- Fonction : Auteur
Oliver J Brady
- Fonction : Auteur
Marc A Suchard
- Fonction : Auteur
Renato Santana Aguiar
- Fonction : Auteur
Nuno R Faria
- Fonction : Auteur
- PersonId : 1253227
- ORCID : 0000-0001-8839-2798
Résumé
Zoonotic viruses that originate in wildlife harm global human health and economic prosperity 1 . Understanding virus transmission at the human-animal-environment interface is a key component of pandemic risk-reduction 2,3 . Zoonotic disease emergence is highest in biodiverse, tropical forests undergoing intensive land-use change 4,5 . Phylodynamic analyses of virus genomes can powerfully test epidemiological hypotheses, but are rarely applied to viruses of animals inhabiting these habitats. Brazil’s densely-populated Atlantic Forest and Cerrado region experienced in 2016–2021 an explosive human outbreak of sylvatic yellow fever, caused by repeated virus spillover from wild neotropical primates 6 . Here we use yellow fever virus (YFV) genome sequences and epidemiological data from neotropical primates, humans, and mosquito vectors to identify the environmental, demographic, and climatic factors determining zoonotic virus spread. Using portable sequencing approaches we generated 498 YFV genomes, resulting in a well-sampled dataset of zoonotic virus genomes sampled from wild mammals. YFV dispersal velocity was slower at higher elevation, in colder regions, and further away from main roads. Virus lineage dispersal was more frequent through wetter areas, areas with high neotropical primate density and through landscapes covered by mosaic vegetation. Higher temperatures were associated with higher virus effective population sizes, and peaks of transmission in warmer, wetter seasons were associated with higher virus evolutionary rates. Our study demonstrates how zoonotic disease transmission is linked to land-use and climate, underscoring the need for One-Health approaches to reducing the rate of zoonotic spillover.
