Gone (and spread) with the birds: Can chorotype analysis highlight the spread of West Nile virus within the Afro-Palaearctic flyway?

Abstract

West Nile virus (WNV) is a globally significant vector-borne disease that is primarily transmitted between birds and mosquitoes. Recently, there has been an increase in WNV in southern Europe, with new cases reported in more northern regions. Bird migration plays a crucial role in the introduction of WNV in distant areas. To better understand and address this complex issue, we adopted a One Health approach, integrating clinical, zoological, and ecological data. We analyzed the role of migratory birds in the Palaearctic-African region in the spread of WNV across Africa and Europe. We categorized bird species into breeding and wintering chorotypes based on their distribution during the breeding season in the Western Palaearctic and the wintering season in the Afrotropical region, respectively. By linking these chorotypes to the occurrence of WNV outbreaks in both continents throughout the annual bird migration cycle, we investigated the relationship between migratory patterns and virus spread. We demonstrate that WNV-risk areas are interconnected through the migration of birds. We identified a total of 61 species that potentially contribute to the intercontinental spread of the virus or its variants, as well as pinpointed high-risk areas for future outbreaks. This interdisciplinary approach, which considers the interconnectedness of animals, humans, and ecosystems, represents a pioneering effort to establish connections between zoonotic diseases across continents. The findings of our study can aid in anticipating the arrival of new WNV strains and predicting the occurrence of other re-emerging diseases. By incorporating various disciplines, we can enhance our understanding of these complex dynamics and provide valuable insights for proactive and comprehensive disease management strategies.

Keywords: Africa; Biogeography; Emerging disease; Europe; Migration; One Health; Pathogeography; Zoonosis.

Fig. 1

West Nile virus in the Afro-Palaearctic. (A) Afro-Palaearctic distribution of WNV human cases. (B) WNV risk model in the Afrotropical realm and the cartographical representation of some explicative variables related to WNV cases.

Fig. 2

Connection of West Nile virus cases and their lineages between Africa and Europe via migratory birds. Breeding (b_Cx) and wintering bird chorotypes (w_Cx) significantly associated with human cases of WNV disease, both in the Western Palaearctic (top maps) and in the Afrotropical realms (bottom maps). Chorotypes are groups of species with statistically similar distribution patterns, irrespective of the habitat they use. Chorotypes may overlap, but their degree of overlap is no greater than randomly expected. The size of the rectangular boxes indicates the number of species forming part of the chorotype. The width of bands connecting Western Palaearctic and Afrotropical chorotypes represents the number of species that are shared by them. Boxes, and bands, are colored according to the WNV lineage associated to the chorotype: blue for lineage 1, red for lineage 2, and violet for lineages 1 and 2. The black box, and its black bands, is the chorotype and its species significantly associated to human cases of WNV disease, but not associated to any lineage. The bird species that belong to each chorotype can be seen in Supplementary Table 5. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)