Ebolavirus evolution and emergence are associated with land use change

Anthropogenic land use change facilitates disease emergence by altering the interface between humans and pathogen reservoirs and is hypothesized to drive pathogen evolution. Here, we show a positive association between land use change and the evolution and dispersal of Zaire ebolavirus (EBOV) and Sudan ebolavirus (SUDV). We update the phylogeographies of EBOV and SUDV, which reveal that the most recent common ancestor of EBOV was circulating around 1960 in the forests of what is now the northwestern Democratic Republic of the Congo, while the most recent common ancestor of SUDV was circulating around 1958 in the southern Sudanese savanna. Both landscapes underwent significant anthropogenic fragmentation between 1940 and 1960, associated with specific colonial "schemes," which substantially altered local human settlement patterns and the surrounding vegetation to support intensive cash crop agriculture. Since these disturbances, landscape fragmentation was spatiotemporally associated with the divergence and dispersal of new variants of both viruses into new ecoregions of Africa. These variants segregated geographically along ecoregion boundaries, resembling a pattern observable for other bat-borne viruses. The amino acid changes which characterized each variant disproportionately involved glycosylation-sensitive amino acids in the surface glycoprotein domain responsible for immune evasion and attachment to host cells, suggesting adaptation to new hosts amidst changing landscapes. Our results show that land use change not only increases the risk of spillover, but also impacts the evolution of viruses themselves. The survey data collected around Gemena, Democratic Republic of the Congo (Montero, 2024), are available in Harvard Dataverse at doi.org. Additional datasets utilized for this research are as follows: History Database of the Global Environment (HYDE) 3.2 (Klein Goldewijk, 2017) available in Data Archiving and Networked Services (DANS) at doi.org (accessed November 28, 2020); Global Forest Watch, Version 1.8, available at storage.googleapis.com (accessed March 28, 2022), with query details for Global Forest Watch data described in Appendix S1: Section S1 under the heading "Global Forest Watch data query."