Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari (Cacajao calvus)

Abstract

Colour vision is highly variable in New World monkeys (NWMs). Evidence for the adaptive basis of colour vision in this group has largely centred on environmental features such as foraging benefits for differently coloured foods or predator detection, whereas selection on colour vision for sociosexual communication is an alternative hypothesis that has received little attention. The colour vision of uakaris (Cacajao) is of particular interest because these monkeys have the most dramatic red facial skin of any primate, as well as a unique fission/fusion social system and a specialist diet of seeds. Here, we investigate colour vision in a wild population of the bald uakari, C. calvus, by genotyping the X-linked opsin locus. We document the presence of a polymorphic colour vision system with an unprecedented number of functional alleles (six), including a novel allele with a predicted maximum spectral sensitivity of 555 nm. This supports the presence of strong balancing selection on different alleles at this locus. We consider different hypotheses to explain this selection. One possibility is that trichromacy functions in sexual selection, enabling females to choose high-quality males on the basis of red facial coloration. In support of this, there is some evidence that health affects facial coloration in uakaris, as well as a high prevalence of blood-borne parasitism in wild uakari populations. Alternatively, the low proportion of heterozygous female trichromats in the population may indicate selection on different dichromatic phenotypes, which might be related to cryptic food coloration. We have uncovered unexpected diversity in the last major lineage of NWMs to be assayed for colour vision, which will provide an interesting system to dissect adaptation of polymorphic trichromacy.

Novel opsin gene variation in large-bodied, diurnal lemurs

“…For five Propithecus species (P. coquereli, P. coronatus, P. deckenii, P. tattersalli and P. verreauxi), we identified the two alleles previously found in lemurs [6] based on variation at site 285 (figure 2): AYA (l max 543 nm) and AYT (l max 558 nm). All spectral sensitivities are based on the estimated effects of differences in the three spectral tuning sites [5,6]. The AYT allele was also found in the single P. perrieri individual.…”

“…Although all three primary sites (180, 277, 285) are variable in polymorphic New World monkeys, variation in lemurs has only been documented in site 285 leading to two alleles: alanine 180, tyrosine 277, alanine 285 (AYA), and alanine 180, tyrosine 277, threonine 285 (AYT), which encode opsins with peak spectral sensitivities (l max ) approximately 543 nm ('M') and approximately 558 nm ('L'), respectively [2][3][4][5][6][7][8]. We sequenced exons 3 and 5 to capture the three key functional sites in the X-linked opsin gene of indriids (electronic supplementary material).…”

“…Polymorphic trichromacy is both widespread and highly variable (more than two opsin alleles) among most diurnal New World monkeys and is found in some day-active Malagasy lemurs (two alleles) [2][3][4][5][6][7][8]. Yet other day-active lemurs appear to have a single opsin allele and are strictly dichromatic [9][10][11].…”

The Genetic and Evolutionary Drives behind Primate Color Vision

“…Atelidae, and Pitheciidae (Perelman et al, 2011), trichromacy appears to have followed the same evolutionary process seen in the Cebinae family (Riba-Hernandez et al, 2004); however, the bald uakari (C. calvus) found in the Pitheciidae family, has recently been reported to have six functional polymorphic L opsin alleles with different combinations of residues at sites 180, 277 and 285, although two of these are estimated to have the λ max at 550 nm (Corso et al, 2016).…”

“…However, it is important to notice that, in many cases, different combinations of residues across the three sites ( (Jacobs and Deegan, 2003a). In the other two families that form the New World monkey parvorder, Data taken from Mollon et al (1984), Travis et al (1988), Boissinot et al (1998), Tan and Li (1999), Jacobs and Deegan (2001, 2003a,b, 2005, Saito et al (2004), Talebi et al (2006), Veilleux and Bolnick (2009), Bunce et al (2011), Corso et al (2016, and Jacobs and Bradley (2016).…”