Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil

Juliana Telles-de-Deus; Ingra M. Claro; Mayara Bertanhe; Charles Whittaker; Márcio Port-Carvalho; Esmenia C. Rocha; Thaís M. Coletti; Camila A.M. da Silva; Ian Nunes Valença; Tamara N. Lima-Camara; Márcia Bicudo de Paula; Mariana S. Cunha; Jaqueline G. de Jesus; Pâmela dos Santos Andrade; Victoria Cox; Natalia C.C.F. de Azevedo; Juliana M. Guerra; Juliana L. Summa; Ana Paula P. Teixeira; Eduardo S. Bergo; Mariza Pereira; Filipe R.R. Moreira; Alvina Clara Felix; Anderson V. de Paula; Raissa H. de Araujo Eliodoro; Marissa da Silva Lima; Franciane M. de Oliveira; Valquíria R. de Souza; Lucas A.M. Franco; Marcelo S. Nardi; Thais C. Sanches; Eric T.B.C. da Silva; Amanda A.C. Coimbra; Paulo R. dos Santos; Katherine Lima de Gouveia; Francisco E.S.P. Vilela; Sarah C. Hill; Dilmar A.G. Oliveira; Hélia M. Piedade; Thaís Guimarães-Luiz; Camila M.G. Abreu; Guilherme Casoni da Rocha; Leandro Abade; William M. de Souza; Ben Lambert; Renato Pereira de Souza; Adriano Pinter; Ester C. Sabino; Luis Filipe Mucci; Nuno R. Faria

doi:10.1038/s41564-026-02302-w

Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil

Juliana Telles-de-Deus
, Ingra M. Claro
, Mayara Bertanhe
, Charles Whittaker
, Márcio Port-Carvalho
, Esmenia C. Rocha
, Thaís M. Coletti
, Camila A.M. da Silva
, Ian Nunes Valença
, Tamara N. Lima-Camara
, Márcia Bicudo de Paula
, Mariana S. Cunha
, Jaqueline G. de Jesus
, Pâmela dos Santos Andrade
, Victoria Cox
, Natalia C.C.F. de Azevedo
, Juliana M. Guerra
, Juliana L. Summa
, Ana Paula P. Teixeira
, Eduardo S. Bergo

Mariza Pereira, Filipe R.R. Moreira, Alvina Clara Felix, Anderson V. de Paula, Raissa H. de Araujo Eliodoro, Marissa da Silva Lima, Franciane M. de Oliveira, Valquíria R. de Souza, Lucas A.M. Franco, Marcelo S. Nardi, Thais C. Sanches, Eric T.B.C. da Silva, Amanda A.C. Coimbra, Paulo R. dos Santos, Katherine Lima de Gouveia, Francisco E.S.P. Vilela, Sarah C. Hill, Dilmar A.G. Oliveira, Hélia M. Piedade, Thaís Guimarães-Luiz, Camila M.G. Abreu, Guilherme Casoni da Rocha, Leandro Abade, William M. de Souza, Ben Lambert, Renato Pereira de Souza, Adriano Pinter, Ester C. Sabino, Luis Filipe Mucci, Nuno R. Faria

Microbiology, Immunology, and Molecular Genetics

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

4 Scopus citations

Abstract

Yellow fever virus (YFV) continues to threaten human and wildlife populations in the Americas, yet its transmission at the forest–urban interface remains unclear. Here we integrate ground- and canopy-level mosquito surveillance, systematic monitoring of non-human primate carcasses and viral metagenomics to describe the dynamics of a sylvatic YFV outbreak in a 186-hectare Atlantic Forest fragment embedded within metropolitan São Paulo, Brazil, between 2017 and 2018. Our analyses reveal that transmission was primarily driven by a single genetic cluster introduced during a period of high abundance of the main vector, Haemagogus leucocelaenus mosquitoes. A near-complete hepatitis A virus genome was detected in a YFV-infected howler monkey, suggesting potential co-infections at the human–wildlife interface. Phylogenetic and epidemiological modelling estimated a basic reproduction number, R₀, for sylvatic yellow fever of 8.2 (95% CI 5.1–12.2), substantially higher than previous estimates for urban outbreaks. Our findings demonstrate that multisource surveillance could provide actionable early warnings in regions at risk for zoonotic spillover.

Original language	English
Pages (from-to)	877-891
Number of pages	15
Journal	Nature Microbiology
Volume	11
Issue number	4
DOIs	https://doi.org/10.1038/s41564-026-02302-w
State	Published - Apr 2026

Bibliographical note

Publisher Copyright:
© The Author(s) 2026.

Funding

We thank the São Paulo State Secretariat for the Environment (2017–2018), including M. Brusadin, L. A. Bucci (Director of PEAL) and P. R. da Silva, for logistical support at PEAL; the Environmental Military Police of São Paulo State and the Metropolitan Civil Guard for operational assistance, particularly during the CADDE Workshop on Viral Metagenomics for Public Health (March 2023) held at PEAL and at the Institute of Tropical Medicine (USP), where preliminary findings were presented; R. Cardoso de Paula (Municipal Health Department of São Paulo) and R. Spinola and H. Sato (State Health Department of São Paulo) for leadership in YFV surveillance and vaccination; D. Fonseca Jr., A. Nepomuceno Duarte (SUCEN, São Paulo State Health Department) and the SUCEN field team for their essential contributions to entomological collections, and P. R. Urbinatti and R. M. Marques Sá de Almeida (Entomology Laboratory of the School of Public Health - USP) for support with taxonomic identification. We acknowledge the use of ERA5-Land meteorological data (Muñoz Sabater, 2019) accessed via the Copernicus Climate Change Service Climate Data Store. The results incorporate modified Copernicus Climate Change Service information (2023); neither the European Commission nor ECMWF is responsible for any use of this information. This work was supported by the Wellcome Trust Digital Technology Development Award (226075/Z/22/Z) (W.M.d.S., N.R.F.); the UK Medical Research Council (MRC) and FAPESP (MRC MR/S0195/1; FAPESP 18/14389-0) (I.M.C., M.B., E.C.S., N.R.F.); the International Pathogen Surveillance Network Catalytic Grant Fund (RT-MeTA, FRMM, ICL, N.R.F.); and the Wellcome Trust Dengue and Zika Immunology and Genomics Multi-Country Network (DeZi Network) (316633/Z/24/Z) (N.R.F., E.C.S.). We also acknowledge support from the MRC Centre for Global Infectious Disease Analysis (MR/X020258/1), funded by the UK MRC (N.R.F.); this UK-funded award is delivered within the Global Health EDCTP3 Joint Undertaking.

Funders	Funder number
FRMM
UK Medical Research Council, Engineering and Physical Sciences Research Council
Entomology Laboratory of the School of Public Health
São Paulo State Health Department
Secretaria Municipal da Saúde Cicade de São Paulo
European Commission
São Paulo State Secretariat for the Environment
Metropolitan Civil Guard
RT-MeTA
WHO International Pathogen Surveillance Network Catalytic Grant Fund
Institut de Cancérologie de Lorraine	MR/X020258/1, 316633/Z/24/Z
Wellcome Trust	226075/Z/22/Z
Fundação de Amparo à Pesquisa do Estado de São Paulo	18/14389-0, MR/S0195/1

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

ASJC Scopus subject areas

Microbiology
Immunology
Applied Microbiology and Biotechnology
Genetics
Microbiology (medical)
Cell Biology

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10.1038/s41564-026-02302-w

Cite this

Telles-de-Deus, J., Claro, I. M., Bertanhe, M., Whittaker, C., Port-Carvalho, M., Rocha, E. C., Coletti, T. M., da Silva, C. A. M., Valença, I. N., Lima-Camara, T. N., Bicudo de Paula, M., Cunha, M. S., de Jesus, J. G., dos Santos Andrade, P., Cox, V., de Azevedo, N. C. C. F., Guerra, J. M., Summa, J. L., Teixeira, A. P. P., ... Faria, N. R. (2026). Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil. Nature Microbiology, 11(4), 877-891. https://doi.org/10.1038/s41564-026-02302-w

@article{fc884eb9708c4d77b54e21c693a04389,

title = "Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil",

abstract = "Yellow fever virus (YFV) continues to threaten human and wildlife populations in the Americas, yet its transmission at the forest–urban interface remains unclear. Here we integrate ground- and canopy-level mosquito surveillance, systematic monitoring of non-human primate carcasses and viral metagenomics to describe the dynamics of a sylvatic YFV outbreak in a 186-hectare Atlantic Forest fragment embedded within metropolitan S{\~a}o Paulo, Brazil, between 2017 and 2018. Our analyses reveal that transmission was primarily driven by a single genetic cluster introduced during a period of high abundance of the main vector, Haemagogus leucocelaenus mosquitoes. A near-complete hepatitis A virus genome was detected in a YFV-infected howler monkey, suggesting potential co-infections at the human–wildlife interface. Phylogenetic and epidemiological modelling estimated a basic reproduction number, R0, for sylvatic yellow fever of 8.2 (95\% CI 5.1–12.2), substantially higher than previous estimates for urban outbreaks. Our findings demonstrate that multisource surveillance could provide actionable early warnings in regions at risk for zoonotic spillover.",

author = "Juliana Telles-de-Deus and Claro, \{Ingra M.\} and Mayara Bertanhe and Charles Whittaker and M{\'a}rcio Port-Carvalho and Rocha, \{Esmenia C.\} and Coletti, \{Tha{\'i}s M.\} and \{da Silva\}, \{Camila A.M.\} and Valen{\c c}a, \{Ian Nunes\} and Lima-Camara, \{Tamara N.\} and \{Bicudo de Paula\}, M{\'a}rcia and Cunha, \{Mariana S.\} and \{de Jesus\}, \{Jaqueline G.\} and \{dos Santos Andrade\}, P{\^a}mela and Victoria Cox and \{de Azevedo\}, \{Natalia C.C.F.\} and Guerra, \{Juliana M.\} and Summa, \{Juliana L.\} and Teixeira, \{Ana Paula P.\} and Bergo, \{Eduardo S.\} and Mariza Pereira and Moreira, \{Filipe R.R.\} and Felix, \{Alvina Clara\} and \{de Paula\}, \{Anderson V.\} and \{de Araujo Eliodoro\}, \{Raissa H.\} and \{da Silva Lima\}, Marissa and \{de Oliveira\}, \{Franciane M.\} and \{de Souza\}, \{Valqu{\'i}ria R.\} and Franco, \{Lucas A.M.\} and Nardi, \{Marcelo S.\} and Sanches, \{Thais C.\} and \{da Silva\}, \{Eric T.B.C.\} and Coimbra, \{Amanda A.C.\} and \{dos Santos\}, \{Paulo R.\} and \{Lima de Gouveia\}, Katherine and Vilela, \{Francisco E.S.P.\} and Hill, \{Sarah C.\} and Oliveira, \{Dilmar A.G.\} and Piedade, \{H{\'e}lia M.\} and Tha{\'i}s Guimar{\~a}es-Luiz and Abreu, \{Camila M.G.\} and \{Casoni da Rocha\}, Guilherme and Leandro Abade and \{de Souza\}, \{William M.\} and Ben Lambert and \{Pereira de Souza\}, Renato and Adriano Pinter and Sabino, \{Ester C.\} and Mucci, \{Luis Filipe\} and Faria, \{Nuno R.\}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2026.",

year = "2026",

month = apr,

doi = "10.1038/s41564-026-02302-w",

language = "English",

volume = "11",

pages = "877--891",

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Telles-de-Deus, J, Claro, IM, Bertanhe, M, Whittaker, C, Port-Carvalho, M, Rocha, EC, Coletti, TM, da Silva, CAM, Valença, IN, Lima-Camara, TN, Bicudo de Paula, M, Cunha, MS, de Jesus, JG, dos Santos Andrade, P, Cox, V, de Azevedo, NCCF, Guerra, JM, Summa, JL, Teixeira, APP, Bergo, ES, Pereira, M, Moreira, FRR, Felix, AC, de Paula, AV, de Araujo Eliodoro, RH, da Silva Lima, M, de Oliveira, FM, de Souza, VR, Franco, LAM, Nardi, MS, Sanches, TC, da Silva, ETBC, Coimbra, AAC, dos Santos, PR, Lima de Gouveia, K, Vilela, FESP, Hill, SC, Oliveira, DAG, Piedade, HM, Guimarães-Luiz, T, Abreu, CMG, Casoni da Rocha, G, Abade, L, de Souza, WM, Lambert, B, Pereira de Souza, R, Pinter, A, Sabino, EC, Mucci, LF & Faria, NR 2026, 'Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil', Nature Microbiology, vol. 11, no. 4, pp. 877-891. https://doi.org/10.1038/s41564-026-02302-w

TY - JOUR

T1 - Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil

AU - Telles-de-Deus, Juliana

AU - Claro, Ingra M.

AU - Bertanhe, Mayara

AU - Whittaker, Charles

AU - Port-Carvalho, Márcio

AU - Rocha, Esmenia C.

AU - Coletti, Thaís M.

AU - da Silva, Camila A.M.

AU - Valença, Ian Nunes

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AU - de Araujo Eliodoro, Raissa H.

AU - da Silva Lima, Marissa

AU - de Oliveira, Franciane M.

AU - de Souza, Valquíria R.

AU - Franco, Lucas A.M.

AU - Nardi, Marcelo S.

AU - Sanches, Thais C.

AU - da Silva, Eric T.B.C.

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AU - dos Santos, Paulo R.

AU - Lima de Gouveia, Katherine

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AU - Sabino, Ester C.

AU - Mucci, Luis Filipe

AU - Faria, Nuno R.

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Evolution and spillover dynamics of yellow fever at the forest–urban interface in Brazil

Abstract

Bibliographical note

Funding

UN SDGs

ASJC Scopus subject areas

Access to Document

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