Contrasting levels of DNA polymorphism at the autosomal and X-linked visual color pigment loci in humans and squirrel monkeys

The X-linked color pigment (opsin) locus is known to be highly polymorphicin the squirrel monkey and other New World monkeys. To see whether this isalso the case for the autosomal (blue) opsin locus, we obtained 32 squirrelmonkey and 30 human blue opsin gene sequences. No amino acid polymorphismwas found in either the squirrel monkey sample or the human sample,contrary to the situation at the X-linked opsin locus. This sharp contrastin the level of polymorphism might be due to differences in gene expressionbetween the autosomal and the X-linked loci. At the X-linked locus,heterozygote advantage can occur because, owing to X-inactivation, the twoalleles in a heterozygote are expressed in different cone cells, producingtwo types of cone cell, whereas at the autosomal locus, heterozygoteadvantage cannot occur because the two alleles in a heterozygote areexpressed in the same cone cells, producing only one type of cone cell(i.e., phenotypically a homozygote). From the sequence data, the levels ofnucleotide diversity (pi, i.e., the number of nucleotide differences persite) are estimated: for the human sample, pi = 0.00% per nondegeneratesite, 0.00% per twofold degenerate site, and 0.04% per fourfold degeneratesite in the coding regions and 0.01% per site in intron 4; for the squirrelmonkey sample, pi = 0.00% per nondegenerate site, 0.00% per twofolddegenerate site, and 0.15% per fourfold degenerate site in the codingregions and 0.17% per site in intron 4. The blue opsin genes from thecommon and pygmy chimpanzees, the gorilla, the capuchin, and the howlermonkey were also sequenced. Features critical to the function of the opsinare well conserved in all known mammalian sequences. However, theinterhelical loops are, on average, actually more conservative than thetransmembrane helical regions. In addition, these sequence data and thosefrom some other genes indicate that the common and pygmy chimpanzees arenot closely related, their divergence data being from one third to one halfthe date of the human-chimpanzee divergence.