Reis-Cunha, J. L.; de Campos Reis, L.; Mendes, L.; Cavalcante, M.; Johansson, M.; McClean, C. J.; Vale Barbosa, G. M. d. G.; Goto, H.; Guerra, J. A.; Jeffares, D. C.

The Amazon is the largest tropical rainforest in the world, and is an important interface between natural rainforest and anthropogenic environments. In the central Amazon region, Leishmania guyanensis is a common agent of cutaneous leishmaniasis (CL), a disfiguring vector-borne disease that circulates between wild mammalian reservoirs and sandfly vectors in sylvatic cycles. People become infected when they interact or disturb this cycle. At present, little is known about the adaptation of Leishmania parasites at the interface between sylvatic and anthropogenic environments. Here, to characterize CL in a transition zone, we conducted a population genomic analysis of 77 Leishmania isolates from human patients living in the outskirts of Manaus or in highways adjacent to the Brazilian Amazon rainforest. We discovered two L. guyanensis populations; an ancestral sylvatic population occurring in densely forested areas far from the city and a derived population, occurring in areas with lower forest cover closer to the city (the city-proximal population). The genomic divergence between these populations indicates that their separation occurred relatively recently, consistent with human-driven development of a new transmission cycle for CL in the Manaus region. The lack of recent gene flow between these populations indicates that the newer city-proximal population has established a transmission cycle that operates independently from ancestral sylvatic transmission. This provides a striking example of the adaptation of disease transmission to an environment that has been altered by human activity.