Abstract
West Nile virus (WNV) has caused repeated large-scale human epidemics in North America since it was first detected in 1999 and is now the dominant vector-borne disease in this continent. Understanding the factors that determine the intensity of the spillover of this zoonotic pathogen from birds to humans (via mosquitoes) is a prerequisite for predicting and preventing human epidemics. We integrated mosquito feeding behavior with data on the population dynamics and WNV epidemiology of mosquitoes, birds, and humans. We show that Culex pipiens, the dominant enzootic (bird-to-bird) and bridge (bird-to-human) vector of WNV in urbanized areas in the northeast and north-central United States, shifted its feeding preferences from birds to humans by 7-fold during late summer and early fall, coinciding with the dispersal of its preferred host (American robins, Turdus migratorius) and the rise in human WNV infections. We also show that feeding shifts in Cx. tarsalis amplify human WNV epidemics in Colorado and California and occur during periods of robin dispersal and migration. Our results provide a direct explanation for the timing and intensity of human WNV epidemics. Shifts in feeding from competent avian hosts early in an epidemic to incompetent humans after mosquito infection prevalences are high result in synergistic effects that greatly amplify the number of human infections of this and other pathogens. Our results underscore the dramatic effects of vector behavior in driving the transmission of zoonotic pathogens to humans.
Highlights
Three quarters of human emerging infectious diseases are caused by zoonotic pathogens [1]
Our data from the mid-Atlantic demonstrate a latesummer shift in the feeding behavior of Cx. pipiens from their preferred avian host, American robins, to humans. This shift offers an explanation for the late-summer timing and increased intensity of human West Nile virus (WNV) epidemics in the northeast and north-central parts of North America [11,29], where this species is the dominant enzootic vector and bridge vector [30]
We have shown that WNV epidemics in the central and western parts of the United States are intensified by feeding shifts that escalate as robins and other WNVcompetent avian hosts disperse and migrate following breeding
Summary
Three quarters of human emerging infectious diseases are caused by zoonotic pathogens [1]. For many of these diseases, nonhuman animals are the primary host and human infections are incidental and often dead-end in nature [1]. These pathogens can have severe consequences for human health, due to high mortality rates, high incidence rates, or both [1,2,3,4]. A critical step in the control of epidemics of zoonotic vector-borne pathogens is determining the feeding preferences of key vectors and how they change over space and time [5]
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