Research Article: Evidence for Co-evolution of West Nile Virus and House Sparrows in North America

Date Published: October 30, 2014

Publisher: Public Library of Science

Author(s): Nisha K. Duggal, Angela Bosco-Lauth, Richard A. Bowen, Sarah S. Wheeler, William K. Reisen, Todd A. Felix, Brian R. Mann, Hannah Romo, Daniele M. Swetnam, Alan D. T. Barrett, Aaron C. Brault, Robert B. Tesh.

Abstract: West Nile virus (WNV) has been maintained in North America in enzootic cycles between mosquitoes and birds since it was first described in North America in 1999. House sparrows (HOSPs; Passer domesticus) are a highly competent host for WNV that have contributed to the rapid spread of WNV across the U.S.; however, their competence has been evaluated primarily using an early WNV strain (NY99) that is no longer circulating. Herein, we report that the competence of wild HOSPs for the NY99 strain has decreased significantly over time, suggesting that HOSPs may have developed resistance to this early WNV strain. Moreover, recently isolated WNV strains generate higher peak viremias and mortality in contemporary HOSPs compared to NY99. These data indicate that opposing selective pressures in both the virus and avian host have resulted in a net increase in the level of host competence of North American HOSPs for currently circulating WNV strains.

Partial Text: West Nile virus (WNV; Flaviviridae) is an arbovirus that was first reported in North America in 1999 in New York. By 2003, the virus had spread to the West Coast. WNV has remained endemic in the U.S. due to the high prevalence of competent Culex spp. mosquito vectors and avian hosts [1]–[4]. The birds considered to be the most important WNV reservoirs are passerines, which are highly susceptible and maintain high viremias for several days during infection [1], [5]. Because infection of Culex vectors is dose dependent, the magnitude of serum viremia in a bird determines its host competence [1], [4], [6].

WNV has evolved to replicate to higher peak titers in HOSPs (Fig. 2) since WNV emergence in North America in the late 1990s. Conversely, the founding East Coast genotype (NY99) has demonstrated a reduced capacity for eliciting infectious titers in HOSPs over time (Fig. 4). Taken together, these observations indicate a cyclic pattern of adaptive selection acting on WNV and avian hosts, suggestive of the ‘Red Queen’ hypothesis of evolution [37]. Mortality and fitness effects of high replication of the founding strain of WNV in HOSPs in North America may have served as a significant selective pressure for increased control of WNV replication in HOSPs that, in turn, may have selected for viral adaptations to increase viremia and therefore transmissibility to mosquitoes. Ultimately, because HOSPs inoculated with WNV only have decreased viremias in response to East Coast viruses that are no longer circulating, the consequence of viral evolution has been an increase in reservoir competence of HOSPs from 1.6 in 2000 to 2.6 in 2013 for extant WNV genotypes (Fig. 3). The Red Queen hypothesis would predict that HOSPs will further adapt to sustain lower viremias in response to WN02 and SW03 genotypes, with corresponding viral mutations selected in order to offset avian antiviral effects.



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