West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior

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.

Figure 1. Cx. pipiens Feeding Patterns, Avian Population Dynamics, and West Nile Virus Epidemiology

(A) Fraction of 148 Cx. pipiens blood meals (±1 SE) from humans and mammals (including humans) identified by PCR and DNA sequencing. (B) Density (birds per hectare) of American robins, density of all birds, and the fraction (±1 SE) of mosquito feedings on robins. (C) Abundance of Culex mosquitoes per trap-night, Culex WNV infection rate (1,000 * infection prevalence, ±1 SE), estimated human WNV infection risk (±1 SE), calculated as the product of mosquito abundance, WNV infection rate, and the time-varying probability of feeding on humans (Human risk) or the June probability, 0.04 (Human risk – no shift), and the number of human WNV cases in Maryland in 2004.

Figure 2. Cx. tarsalis Feeding Patterns, Avian Population Dynamics, and West Nile Virus Epidemiology

Fraction of Cx. tarsalis feedings from mammals (±1 SE), abundances of American robins [birds/survey in (A), birds/hectare ±1 SD in (B)], and the number of human WNV cases in 2004 in California (A) and Colorado (B).