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Int J Primatol. 2014;35:71-87. Epub 2013 Aug 23.

Color Vision Variation as Evidenced by Hybrid L/M Opsin Genes in Wild Populations of Trichromatic Alouatta New World Monkeys.

Author information

1
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Kashiwanoha, Kashiwa, Chiba 277-8562 Japan.
2
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Kashiwanoha, Kashiwa, Chiba 277-8562 Japan ; Department of Anatomy, Kitasato University School of Medicine, Minami-ku, Sagamihara, Kanagawa 252-0374 Japan.
3
Department of Anthropology, State University of New York at Geneseo, Geneseo, New York 14454 USA.
4
Department of Anthropology, University of Calgary, 2500 University Drive N.W., Calgary, Alberta T2N 1N4 Canada.

Abstract

Platyrrhine (New World) monkeys possess highly polymorphic color vision owing to allelic variation of the single-locus L/M opsin gene on the X chromosome. Most species consist of female trichromats and female and male dichromats. Howlers (genus Alouatta) are an exception; they are considered to be routinely trichromatic with L and M opsin genes juxtaposed on the X chromosome, as seen in catarrhine primates (Old World monkeys, apes, and humans). Yet it is not known whether trichromacy is invariable in howlers. We examined L/M opsin variation in wild howler populations in Costa Rica and Nicaragua (Alouatta palliata) and Belize (A. pigra), using fecal DNA. We surveyed exon 5 sequences (containing the diagnostic 277th and 285th residues for λmax) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λmax) of the reconstituted L and M opsin photopigments were 564 nm and 532 nm, respectively, in both species. We found one M-L hybrid sequence with a recombinant 277/285 haplotype in Alouatta palliata and two L-M hybrid sequences in A. pigra. The λmax values of the reconstituted hybrid photopigments were in the range of 546~554 nm, which should result in trichromat phenotypes comparable to those found in other New World monkey species. Our finding of color vision variation due to high frequencies of L/M hybrid opsin genes in howlers challenges the current view that howlers are routine and uniform trichromats. These results deepen our understanding of the evolutionary significance of color vision polymorphisms and routine trichromacy and emphasize the need for further assessment of opsin gene variation as well as behavioral differences among subtypes of trichromacy.

KEYWORDS:

Anomalous trichromacy; Color vision; Howlers; Polymorphism

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