Ecological divergence of two sympatric lineages of Buggy Creek virus, an arbovirus associated with birds.

Most arthropod-borne viruses (arboviruses) show distinct serological subtypes or evolutionary lineages, with the evolution of different strains often assumed to reflect differences in ecological selection pressures. Buggy Creek virus (BCRV) is an unusual RNA virus (Togaviridae, Alphavirus) that is associated primarily with a cimicid swallow bug (Oeciacus vicarius) as its vector and the Cliff Swallow (Petrochelidon pyrrhonota) and the introduced House Sparrow (Passer domesticus) as its amplifying hosts. There are two sympatric lineages of BCRV (lineages A and B) that differ from each other by > 6% at the nucleotide level. Analysis of 385 BCRV isolates all collected from bug vectors at a study site in southwestern Nebraska, USA, showed that the lineages differed in their peak times of seasonal occurrence within a summer. Lineage A was more likely to be found at recently established colonies, at those in culverts (rather than on highway bridges), and at those with invasive House Sparrows, and in bugs on the outsides of nests. Genetic diversity of lineage A increased with bird colony size and at sites with House Sparrows, while that of lineage B decreased with colony size and was unaffected by House Sparrows. Lineage A was more cytopathic on mammalian cells than was lineage B. These two lineages have apparently diverged in their transmission dynamics, with lineage A possibly more dependent on birds and lineage B perhaps more a bug virus. The long-standing association between Cliff Swallows and BCRV may have selected for immunological resistance to the virus by swallows and thus promoted the evolution of the more bug-adapted lineage B. In contrast, the recent arrival of the introduced House Sparrow and its high competence as a BCRV amplifying host may be favoring the more bird-dependent lineage A.