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Trade-offs shaping transmission of sylvatic dengue and Zika viruses in monkey hosts

Author

Listed:
  • Kathryn A. Hanley

    (New Mexico State University)

  • Hélène Cecilia

    (New Mexico State University)

  • Sasha R. Azar

    (University of Texas Medical Branch
    Houston Methodist Research Institute, Houston Methodist Hospital)

  • Brett A. Moehn

    (New Mexico State University)

  • Jordan T. Gass

    (New Mexico State University)

  • Natalia I. Oliveira da Silva

    (University of Texas Medical Branch)

  • Wanqin Yu

    (New Mexico State University)

  • Ruimei Yun

    (University of Texas Medical Branch)

  • Benjamin M. Althouse

    (New Mexico State University
    University of Washington)

  • Nikos Vasilakis

    (University of Texas Medical Branch
    University of Texas Medical Branch
    University of Texas Medical Branch)

  • Shannan L. Rossi

    (University of Texas Medical Branch
    University of Texas Medical Branch
    University of Texas Medical Branch
    University of Texas Medical Branch)

Abstract

Mosquito-borne dengue (DENV) and Zika (ZIKV) viruses originated in Old World sylvatic (forest) cycles involving monkeys and canopy-living Aedes mosquitoes. Both viruses spilled over into human transmission and were translocated to the Americas, opening a path for spillback into Neotropical sylvatic cycles. Studies of the trade-offs that shape within-host dynamics and transmission of these viruses are lacking, hampering efforts to predict spillover and spillback. We infected a native, Asian host species (cynomolgus macaque) and a novel, American host species (squirrel monkey) with sylvatic strains of DENV-2 or ZIKV via mosquito bite. We then monitored aspects of viral replication (viremia), innate and adaptive immune response (natural killer (NK) cells and neutralizing antibodies, respectively), and transmission to mosquitoes. In both hosts, ZIKV reached high titers that translated into high transmission to mosquitoes; in contrast DENV-2 replicated to low levels and, unexpectedly, transmission occurred only when serum viremia was below or near the limit of detection. Our data reveal evidence of an immunologically-mediated trade-off between duration and magnitude of virus replication, as higher peak ZIKV titers are associated with shorter durations of viremia, and higher NK cell levels are associated with lower peak ZIKV titers and lower anti-DENV-2 antibody levels. Furthermore, patterns of transmission of each virus from a Neotropical monkey suggest that ZIKV has greater potential than DENV-2 to establish a sylvatic transmission cycle in the Americas.

Suggested Citation

  • Kathryn A. Hanley & Hélène Cecilia & Sasha R. Azar & Brett A. Moehn & Jordan T. Gass & Natalia I. Oliveira da Silva & Wanqin Yu & Ruimei Yun & Benjamin M. Althouse & Nikos Vasilakis & Shannan L. Rossi, 2024. "Trade-offs shaping transmission of sylvatic dengue and Zika viruses in monkey hosts," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46810-x
    DOI: 10.1038/s41467-024-46810-x
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    References listed on IDEAS

    as
    1. Rotem Ben-Shachar & Katia Koelle, 2018. "Transmission-clearance trade-offs indicate that dengue virulence evolution depends on epidemiological context," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Benjamin M. Althouse & Mathilde Guerbois & Derek A. T. Cummings & Ousmane M. Diop & Ousmane Faye & Abdourahmane Faye & Diawo Diallo & Bakary Djilocalisse Sadio & Abdourahmane Sow & Oumar Faye & Amadou, 2018. "Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    3. Alizon, Samuel & van Baalen, Minus, 2008. "Transmission–virulence trade-offs in vector-borne diseases," Theoretical Population Biology, Elsevier, vol. 74(1), pages 6-15.
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