ORIGIN AND MOLECULAR EVOLUTION OF THE X-LINKED DUPLICATE COLOR-VISIONGENES IN HOWLER MONKEYS

Like humans and Old World monkeys (OWMs), the howler monkeys, a genus of New World monkeys (NWMs), have trichromatic vision because they pos sess 1 autosomal (blue pigment) and 2 X-linked (red and green pigments ) color vision genes. In contrast, the other NWM species investigated in detail have only 1 autosomal and 1 X-linked color vision gene, thou gh the X-linked locus is polymorphic with 3 alleles. To understand the origin of trichromacy in howler monkeys, several NWM species were exa mined for the number of X-linked pigment loci, and intron 4, and exons 3, 4, and 5 of the red and green pigment genes of a male howler monke y were sequenced. The spider monkey, the woolly monkey, the saki monke y, and the bearded saki monkey were shown by the technique of single s trand conformational polymorphism (SSCP) and by Southern blotting to h ave only 1 X-linked color vision gene, suggesting that within NWMs, th e howler monkeys are the only genus with 2 X-linked pigment loci. The sequences of exons 3, 4, and 5 and intron 4 reveal that the gene dupli cation in the howler monkey was independent of that in the human-ape-O WM lineage. In addition, the amino acids at 4 critical sites for spect ral tuning suggest that the duplication in the common ancestor of howl er monkeys was derived from the incorporation of 2 alleles that were, respectively, very similar to the P535 (green) and P562 (red) pigment alleles currently existing in the squirrel monkey and capuchin (2 NWWM genera). This hypothesis implies that the P535-P562 polymorphism exis ted before the platyrrhini (NWM) radiation, which took place about 20 million years ago. Furthermore, the distribution of sequence differenc es in intron 4 between the 2 howler monkey genes suggests that the 2 i ntron 4 sequences have been homogenized by recent gene conversion even ts, providing further evidence for the frequent occurrence of gene con version between X-linked pigment genes.