Stronger population differentiation at infection-sensing than infection-clearing innate immune loci in songbirds: Different selective regimes for different defenses

Abstract

Parasite-mediated selection is widespread at loci involved in immune defense, but different defenses may experience different selective regimes. For defenses involved in clearing infections, purifying selection favoring a single most efficacious allele likely predominates. However, for defenses involved in sensing and recognizing infections, evolutionary arms races may make positive selection particularly important. This could manifest primarily within populations (e.g., balancing selection maintaining variation) or among them (e.g., spatially varying selection enhancing population differences in allele frequencies). We genotyped three toll-like receptors (TLR; involved in sensing infections) and three avian beta-defensins (involved in clearing infections) in 96 song sparrows (Melospiza melodia) from three breeding populations that differ in disease resistance. Variation-based indicators of selection (proportion of variable sites, proportion of nonsynonymous SNPs, proportion of sites bearing signatures of positive or purifying selection, rare allele frequencies) did not differ appreciably between the two locus types. However, differentiation was generally higher at infection-sensing than infection-clearing loci. Allele frequencies differed markedly at TLR3, driven by a variant predicted to alter protein function. Geographically structured variants at infection-sensing loci may reflect local adaptation to spatially heterogeneous parasite communities. Selective regimes experienced by infection-sensing versus infection-clearing loci may differ primarily due to parasite-mediated population differentiation.

Keywords: AvBD; TLR; functional role hypothesis; geographic variation; positive selection; purifying selection.