Polygenic viral factors enable efficient mosquito-borne transmission of African Zika virus

Shiho Torii, Jennifer S. Lord, Morgane Lavina, Matthieu Prot, Alicia Lecuyer, Cheikh T. Diagne, Oumar Faye, Ousmane Faye, Amadou A. Sall, Michael B. Bonsall, Etienne Simon-Lorière, Xavier Montagutelli and Louis Lambrechts ()
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Shiho Torii: Insect-Virus Interactions Unit
Jennifer S. Lord: Liverpool School of Tropical Medicine
Morgane Lavina: Insect-Virus Interactions Unit
Matthieu Prot: Evolutionary Genomics of RNA Viruses Unit
Alicia Lecuyer: Insect-Virus Interactions Unit
Cheikh T. Diagne: Institut Pasteur de Dakar
Oumar Faye: Institut Pasteur de Dakar
Ousmane Faye: Institut Pasteur de Dakar
Amadou A. Sall: Institut Pasteur de Dakar
Michael B. Bonsall: University of Oxford
Etienne Simon-Lorière: Evolutionary Genomics of RNA Viruses Unit
Xavier Montagutelli: Mouse Genetics Laboratory
Louis Lambrechts: Insect-Virus Interactions Unit

Nature Communications, 2025, vol. 16, issue 1, 1-17

Abstract: Abstract Zika virus (ZIKV) is a mosquito-borne orthoflavivirus primarily transmitted among humans by Aedes aegypti. Over the past two decades, it has caused significant outbreaks associated with birth defects and neurological disorders. ZIKV consists of two main genotypes: the African and Asian lineages, each exhibiting distinct biological properties. African lineage strains are transmitted more efficiently by mosquitoes, but the genetic basis for this difference has been elusive. Here, we investigate this question by comparing recent African and Asian strains using chimeric viruses with swapped genome segments. Our results show that structural genes from the African strain enhance viral internalization, while non-structural genes improve genome replication and infectious particle production in mosquito cells. In vivo mosquito transmission is most significantly influenced by structural genes, although no single viral gene alone is decisive. We also develop a stochastic model of in vivo viral dynamics that reflects the observed patterns, suggesting the key difference between African and Asian strains lies in their ability to traverse mosquito salivary glands. Our findings imply the polygenic nature of ZIKV transmissibility has hindered Asian strains from achieving the same transmission efficiency as African strains, highlighting the role of lineage-specific adaptive landscapes in ZIKV evolution and emergence.

Date: 2025
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DOI: 10.1038/s41467-025-64627-0

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