Trans‐specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates

Abstract

Many New World (NW) primates possess a remarkable polymorphism in an X-linked locus, which encodes for the visual pigments (opsins) used for colour vision. Females that are heterozygous for opsin alleles of different spectral sensitivity at this locus have trichromatic colour vision, whereas homozygous females and males are dichromatic, with poor colour discrimination in the red-green range. Here we describe an extensive survey of allelic variation in both exons and introns at this locus within and among species of the Callitrichines (marmosets and tamarins). All five genera of Callitrichines have the X-linked polymorphism, and only the three functional allelic classes described previously (with maximum wavelength sensitivities at about 543 nm, 556 nm and 563 nm) were found among the 16 species and 233 or more X-chromosomes sampled. In spite of the homogenizing effects of gene conversion, phylogenetic analyses provide direct evidence for trans-specific evolution of alleles over time periods of at least 5-6 million years, and up to 14 million years (estimated from independent phylogenies). These conclusions are supported by the distribution of insertions and deletions in introns. The maintenance of polymorphism over these time periods requires an adaptive explanation, which must involve a heterozygote advantage for trichromats. The lack of detection of alleles that are recombinant for spectral sensitivity suggests that such alleles are suboptimal. The two main hypotheses for the selective advantage of trichromacy in primates are frugivory for ripe fruits and folivory for young leaves. The latter can be discounted in Callitrichines, as they are not folivorous.

Scan of Human Genome Reveals No New Loci Under Ancient Balancing Selection

“…Red asterisks indicate the MAXDIV of the 16 loci for which we obtained extended sequence. experimental literature on balancing selection, there are only three well-documented instances of transspecies balancing selection among eukaryotes: (i) the MHC (Hughes and Yeager 1998), (ii) the gene responsible for middle-wavelength and long-wavelength color vision in New World monkeys (Surridge and Mundy 2002), and (iii) the self-incompatibility (SI) loci in plants, which have arisen independently multiple times (Castric and Vekemans 2004). Beyond these examples, one could argue that the sex chromosomes, which have arisen multiple times (Fraser and Heitman 2005), are the oldest and most prevalent example of balancing selection.…”

Bare skin, blood and the evolution of primate colour vision

“…One of the main contributions we make here is the argument that colour vision is near-optimal for discriminating skin colour modulations, something that increases the prima facie plausibility of the hypothesis that trichromacy was originally selected for the perception of skin colour signalling. Other adaptive explanations have been put forth to explain primate colour vision, including advantages for frugivory (Allen 1879;Mollon 1989;Osorio & Vorobyev 1996;Regan et al 2001;Surridge & Mundy 2002), and for folivory (Lucas et al 2003). Our discussion here provides no answer as to which of these may more likely have been the original selection pressure for trichromacy, or whether all these hypotheses may be important contributors (Regan et al 2001).…”

The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinusspp.)

“…DNA was extracted from plucked hair samples from each individual tamarin using a QIAamp DNA mini-kit (Qiagen, Crawley, UK). PCR and sequence analysis of exons 3, 4 and 5 were performed as previously described (Surridge and Mundy, 2002). Genotypes were assigned according to the combined sequence of the four important amino acids in each of the exons mentioned above.…”