Color vision diversity and significance in primates inferred from genetic and field studies

Abstract

Color provides a reliable cue for object detection and identification during various behaviors such as foraging, mate choice, predator avoidance and navigation. The total number of colors that a visual system can discriminate is largely dependent on the number of different spectral types of cone opsins present in the retina and the spectral separations among them. Thus, opsins provide an excellent model system to study evolutionary interconnections at the genetic, phenotypic and behavioral levels. Primates have evolved a unique ability for three-dimensional color vision (trichromacy) from the two-dimensional color vision (dichromacy) present in the majority of other mammals. This was accomplished via allelic differentiation (e.g. most New World monkeys) or gene duplication (e.g. Old World primates) of the middle to long-wavelength sensitive (M/LWS, or red-green) opsin gene. However, questions remain regarding the behavioral adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive color vision variability in New World monkeys, where trichromats and dichromats are found in the same breeding population, enabling us to directly compare visual performances among different color vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioral context. I shall summarize recent findings on color vision evolution in primates and introduce our genetic and behavioral study of vision-behavior interrelationships in free-ranging sympatric capuchin and spider monkey populations in Costa Rica.

Keywords: Color vision; New World monkeys; Opsin; Primates.

Fig. 1

L/M opsin subtypes in primates distinguished on the basis of the ‘three-sites’ composition. At each amino acid site, longer-wave residue (S at 180, Y at 277, T at 285) is indicated with red and the shorter-wave residue (A at 180, F at 277, A at 285) is indicated with green. The expected λ_max values are given to each subtype according to the ‘three-sites’ rule. The major five subtypes found in Platyrrhini are boldfaced and other subtypes are indicated with smaller font. In Lemuriformes, only four species (Varecia variegata, V. rubra, Propithecus coquereli, and Eulemur macaco flavifrons) have been reported to retain two subtypes as alleles, while other species examined to date have either one of the two (Heesy and Ross ; Jacobs et al. ; Jacobs and Deegan ; Tan and Li ; Veilleux and Bolnick 2009). In Tarsiiformes, extant species have either one of the two subtypes but their common ancestral species is suspected to have had both subtypes as alleles (Melin et al. ; Tan and Li 1999). In Pitheciidae of New World monkeys (NWM), six alleles have been found from bald uakari (Cacajao calvus) (Corso et al. 2016). In Atelinae of NWM, λ_max values of SYT, SFT and AFT are significantly short-wave shifted (λ_max indicated in parentheses) from the expectation due to additional mutations and are highlighted with blue (Matsumoto et al. 2014). In Atelinae, two alleles are typically found in each species: SYT and SFT in Ateles, SYT and AFT in Lagothrix lagotricha (Matsumoto et al. 2014) and SYT and SFT in Brachyteles (AFA is only found in Brachyteles hypoxanthus) (Talebi et al. 2006). In Alouattinae, AFT and SYA are recombinant variants recently reported (Matsushita et al. 2014). In Old World monkeys (OWM) and apes, SFA is reported as a rare recombinant variant in a macaque species Macaca fascicularis (Onishi et al. 1999, 2002) and in chimpanzee Pan troglodytes (Terao et al. 2005). In humans, a variety of variants are reported (Deeb ; Hayashi et al. 2006). AYT is reported as a rare recombinant variant for Saimiri boliviensis in Cebinae (Cropp et al. 2002) but omitted here for simplicity