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.