Molecular evolution of colour vision in primates

Abstract

Trichromacy in catarrhine primates has evolved from the ancestral dichromatic state of other mammals through a duplication of the longwave-sensitive (LWS) opsin gene on the X chromosome. The duplicate genes encode for L and M pigment variants with l max values at 565 and 535 nm respectively; the amino acid differences responsible for this spectral shift are at sites 180, 277 and 285. Upstream of this gene array is a locus control region (LCR) which appears to determine via interactions with the minimal promoter region which gene (L or M) is selected for expression. Gene conversion is a feature of the array with the L and M genes showing a high level of sequence identity. In contrast, trichromacy in platyrrhine primates is based on a single polymorphic LWS gene on the X chromosome that specifies pigments with l max values from 565 to 530 nm. This spectral variation again arises from substitutions at sites 180, 277 and 285. Multiple alleles at this locus are found in many species, with trichromacy limited to females that inherit two different alleles. The exception is the howler monkey that follows the catarrhine model with duplicate LWS genes and full trichromacy. The duplication in the howler monkey is however clearly different from that in catarrhines as it includes the LCR in the duplicated segment. Amongst the prosimians, a polymorphic LWS gene has been found in some members of the lemur family. The primate SWS1 pigment peaks in the violet region of the spectrum. This shift from ancestral UV-sensitivity is largely due to substitution at sites 86 and 93, with Pro93 present in all primates and Leu86 in tarsiers, platyrrhines and catarrhines. Site 86 is however much more variable amongst the lemurs with either Ser, Cys, or Val present, indicating a separate origin for violet-sensitivity in this group. Surprisingly, the Aye-Aye has Phe86, the residue present in UV pigments, indicating that UV-sensitivity may be present in this unique species.