Molecular evolution of trichromacy in primates

Abstract

Although trichromacy in Old and New World primates is based on three visual pigments with spectral peaks in the violet (SW, shortwave), green (MW, middlewave) and yellow-green (LW, longwave) regions of the spectrum, the underlying genetic mechanisms differ. The SW pigment is encoded in both cases by an autosomal gene and, in Old World primates, the MW and LW pigments by separate genes on the X chromosome. In contrast, there is a single polymorphic X-linked gene in most New World primates with three alleles coding for spectrally distinct pigments. The one reported exception to this rule is the New World howler monkey that follows the Old World system of separate LW and MW genes. A comparison of gene sequences in these different genetic systems indicates that the duplication that gave rise to the separate MW and LW genes of Old World primates is more ancient than that in the howler monkey. In addition, the amino acid sequences of the two howler monkey pigments show similarities to the pigments encoded by the polymorphic gene of other New World primates. It would appear therefore that the howler monkey gene duplication arose after the split between New and Old World primates and was generated by an unequal crossover that placed two different forms of the New World polymorphic gene on to a single chromosome. In contrast, the lack of identity at variable sites within the New and Old World systems argues for the origin of the separate genes in Old World primates by the duplication of a single form of the gene followed by divergence to give spectrally distinct LW and MW pigments. In contrast, the similarity in amino acid variation across the tri-allelic system of New World primates indicates that this polymorphism had a single origin in New World primates. A striking feature of all these pigments is the use of a common set of substitutions at three amino acid sites to achieve the spectral shift from MW at around 530 nm to LW at around 560 nm. The separate origin of the trichromacy in New and Old World primates would indicate that the selection of these three sites is the result of convergent evolution, perhaps as a consequence of visual adaptation in both cases to foraging for yellow and orange fruits against a green foliage.

Genome of the Chinese tree shrew

“…The tree shrew genome encompasses the orthologues of almost all the 209 known visually related human genes, but lacks two cone photoreceptors, the middle wave-length sensitive proteins, which are specifically duplication genes in catarrhines and lead to the trichromacy in higher primates 28 . The absence of the middle wave-length sensitive proteins is consistent with the fact that tree shrews, similar to some lower primates, lack the green pigment and possess dichromats 29 . As most tree shrew species are diurnal and spend the entire night for sleep in their nests, they do not rely on dim-light visuals 29 .…”

“…The absence of the middle wave-length sensitive proteins is consistent with the fact that tree shrews, similar to some lower primates, lack the green pigment and possess dichromats 29 . As most tree shrew species are diurnal and spend the entire night for sleep in their nests, they do not rely on dim-light visuals 29 . The evolutionary rate testing suggested that the rod photoreceptor rhodopsin, which is responsible for the night vision, had a faster evolutionary rate in the tree shrew lineage (Supplementary Fig.…”

Relaxed selective pressure on an essential component of pheromone transduction in primate evolution

“…We presume that, at a certain point in human evolution, ancestral species may have relied more on visual and auditory signals, rather than on chemical signals, for communicating social and reproductive status. Remarkably, it is at the time in evolution when selective pressure on TRPC2 is relaxed that the common ancestor of OW monkeys and apes developed trichromatic color vision through a gene duplication of the green͞red opsin gene (32,33). Indeed, many species of OW monkeys signal sexual and social status via colorful skin pigmentation of the face or genitalia.…”

Optimal mechanisms for finding and selecting mates: how threespine stickleback ( Gasterosteus aculeatus ) should encode male throat colors

“…One of the most studied signal/receiver systems in this regard is the color vision of insect pollinators and the flowers with which they interact (Chittka 1996;Chittka 1997;Chittka and Briscoe 2001 The evolutionary history we are trying to untangle is potentially paralleled not only by insects and flowers. Similar scenarios may be proposed, for instance, for primates and fruit; did trichromacy evolve in primates to aid in detecting and selecting ripened fruit (Hunt et al 1998;Mollon 1989;Osorio and Vorobyev 1996;Regan et al 1998;Smith et al 2003), or did fruit color evolve to attract seed dispersers more effectively? Our proposal that the relevant component of variation in throat color should be represented along a line through color space may provide useful insight into many such similar questions concerning the evolution of signals and receivers.…”