Host heterogeneity dominates West Nile virus transmission

Abstract

Heterogeneity in host populations and communities can have large effects on the transmission and control of a pathogen. In extreme cases, a few individuals give rise to the majority of secondary infections, which have been termed super spreading events. Here, we show that transmission of West Nile virus (WNV) is dominated by extreme heterogeneity in the host community, resulting in highly inflated reproductive ratios. A single relatively uncommon avian species, American robin (Turdus migratorius), appeared to be responsible for the majority of WNV-infectious mosquitoes and acted as the species equivalent of a super spreader for this multi-host pathogen. Crows were also highly preferred by mosquitoes at some sites, while house sparrows were significantly avoided. Nonetheless, due to their relative rarity, corvids (crows and jays) were relatively unimportant in WNV amplification. These results challenge current beliefs about the role of certain avian species in WNV amplification and demonstrate the importance of determining contact rates between vectors and host species to understand pathogen transmission dynamics.

Figure 1

(a) Relative abundance of birds at two residential sites and three urban sites. For scientific names see AOU (2005). (b) Percent of avian feedings from each host species based on identification of Culex mosquito blood meals by PCR amplification of the cytochrome b gene followed by DNA sequencing. Sample size of mosquito feedings in parentheses. (c) Feeding indices of Culex mosquitoes and 95% CI. Positive values are preferences; negative values designate avoidance and are calculated as (−1/P_i). Columns with an asterisk are minimum avoidance estimates (see §2). All preferences, except hatched columns, are significantly different from 1 (two-tailed p<0.05; all robin preferences p<0.0001). (d) Amplification fraction (proportion of abundance×feeding preference×reservoir competence) of each species, a surrogate for the fraction of West Nile virus infectious mosquitoes resulting from feeding on that avian host.

Figure 1

(a) Relative abundance of birds at two residential sites and three urban sites. For scientific names see AOU (2005). (b) Percent of avian feedings from each host species based on identification of Culex mosquito blood meals by PCR amplification of the cytochrome b gene followed by DNA sequencing. Sample size of mosquito feedings in parentheses. (c) Feeding indices of Culex mosquitoes and 95% CI. Positive values are preferences; negative values designate avoidance and are calculated as (−1/P_i). Columns with an asterisk are minimum avoidance estimates (see §2). All preferences, except hatched columns, are significantly different from 1 (two-tailed p<0.05; all robin preferences p<0.0001). (d) Amplification fraction (proportion of abundance×feeding preference×reservoir competence) of each species, a surrogate for the fraction of West Nile virus infectious mosquitoes resulting from feeding on that avian host.

Figure 2

Relative reproductive ratios, R_0,rel, resulting from host heterogeneity in mosquito feeding and reservoir competence and the date in 2004 that WNV was first detected in mosquitoes.