Assortative mating at the innate immune locus TLR3 in song sparrows: opposites do not attract

Parasites impose strong selection on the immune genes of their hosts. Much of what we know about the evolutionary ecology of immune genes comes from studies of the major histocompatibility complex (MHC), whose products recognize nonself-antigens and initiate an adaptive immune response. MHC loci are remarkably polymorphic, due in part to widespread nonrandom (generally disassortative) mating. At innate immune loci, however, it remains an open question whether nonrandom mating occurs and, if so, whether mating is assortative or disassortative. We sequenced wild-breeding song sparrows, Melospiza melodia , at part of the extracellular domain of Toll-like receptor 3 ( TLR3 ), an innate immune locus that detects viral infection and varies geographically across song sparrow populations. Social mates were more similar at TLR3 than potential mates (i.e. cross-sex pairs of individuals not mated to one another). By contrast, social mates did not differ from potential mates in neutral-locus (microsatellite) genetic similarity. This is the first evidence, to our knowledge, that innate immune loci may be targets of nonrandom mating. Assortative mating at TLR3 could be adaptive if homozygotes have a fitness advantage, perhaps involving enhanced dimerization. We conclude that (1) nonrandom mating with respect to immune genotype is not restricted to genes of the MHC and (2) individual genetic variation at TLR3 in this population appears to be maintained despite, not because of, patterns of mate choice. • We examined whether nonrandom mating occurs at innate immune loci in song sparrows. • Social pairs were more genetically similar than random male–female pairs at TLR3. • Social pairs were not more similar at neutral loci (microsatellites). • Ours is the first demonstration of nonrandom mating based on non-MHC immune loci. • TLR3 variation is presumably maintained despite, not because of, mate choice patterns.