Natural selection on the olfactory receptor gene family in humans and chimpanzees

Abstract

The olfactory receptor (OR) genes constitute the largest gene family in mammalian genomes. Humans have >1,000 OR genes, of which only approximately 40% have an intact coding region and are therefore putatively functional. In contrast, the fraction of intact OR genes in the genomes of the great apes is significantly greater (68%-72%), suggesting that selective pressures on the OR repertoire vary among these species. We have examined the evolutionary forces that shaped the OR gene family in humans and chimpanzees by resequencing 20 OR genes in 16 humans, 16 chimpanzees, and one orangutan. We compared the variation at the OR genes with that at intergenic regions. In both humans and chimpanzees, OR pseudogenes seem to evolve neutrally. In chimpanzees, patterns of variability are consistent with purifying selection acting on intact OR genes, whereas, in humans, there is suggestive evidence for positive selection acting on intact OR genes. These observations are likely due to differences in lifestyle, between humans and great apes, that have led to distinct sensory needs.

Figure  1

Ka/Ks values for OR genes and pseudogenes in human and chimpanzee. Values for polymorphic and fixed sites are plotted as unblackened and blackened bars, respectively.

Figure  2

Marginal posterior distribution of the directional selection parameter (γ=2N_es) on amino acid replacement mutations. A, Chimpanzee intact OR genes and pseudogenes. B, Human intact OR genes and pseudogenes.

Figure  3

The joint distribution of γ and logω, as estimated from the MCMC scheme. A, Chimpanzee OR pseudogenes. B, Chimpanzee intact OR genes. C, Human OR pseudogenes. D, Human intact OR genes.

Figure  4

Joint distribution of the scaled selection coefficient (2Ns) that is associated with mutations in OR genes and species divergence parameters (in units of τ).

Figure  5

Three OR genes studied on human chromosome 11. Rectangles represent the OR coding regions along the chromosome. Indicated are P value of the H test, P(H); Tajima’s D value; and nucleotide diversity, π.