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The  killer-cell immunoglobulin-like receptor  ( KIR ) region comprises a fast-evolving family of genes that encode receptors for natural killer (NK) cells and have crucial role in host defense. Evolution of  KIR  was examined in the context of the human genome. Gene-content diversity and single nucleotide polymorphisms (SNP) in the  KIR  genes and flanking regions were compared to >660,000 genome-wide SNPs in over 800 individuals from 52 populations of the human genome diversity panel (HGDP).  KIR  allelic diversity was further examined using next generation sequencing in a subset of 56 individuals. We identified the SNP  rs587560  located in  KIR3DL3  as a marker of  KIR2DL2  and  KIR2DL3  and, consequently, Cen A and Cen B haplotypes. We also show that combinations of two  KIR2DL4  SNPs ( rs35656676  and  rs592645 ) distinguish  KIR3DL1  from  KIR3DS1  and also define the major  KIR3DL1  high- and low-expressing alleles lineages. Comparing the diversity of the SNPs within the  KIR  region to remainder of the genome, we observed a high diversity for the centromeric  KIR  region consistent with balancing selection ( p  < 0.01); in contrast, centromeric  KIR  diversity is significantly reduced in East Asian populations ( p  < 0.01), indicating purifying selection. By analyzing SNP haplotypes in a region spanning ~500 kb that includes the  KIR  cluster, we observed evidence of strong positive selection in Africa for high-expressing  KIR3DL1  alleles, favored over the low-expressing alleles ( p  < 0.01). In sharp contrast, the strong positive selection ( p  < 0.01) that we also observed in the telomeric  KIR  region in Oceanic populations tracked with a high frequency of  KIR3DS1 . In addition, we demonstrated that worldwide frequency of high-expression  KIR3DL1  alleles was correlated with virus with virus (r = 0.64,  p  < 10 −6 ) and protozoa (r = 0.69,  p  < 10 −6 ) loads, which points to selection globally on  KIR3DL1  high-expressing alleles attributable to pathogen exposure.

Fluctuating and Geographically Specific Selection Characterize Rapid Evolution of the Human KIR Region