Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates

Abstract

Olfactory receptor (OR) genes constitute the molecular basis for the sense of smell and are encoded by the largest gene family in mammalian genomes. Previous studies suggested that the proportion of pseudogenes in the OR gene family is significantly larger in humans than in other apes and significantly larger in apes than in the mouse. To investigate the process of degeneration of the olfactory repertoire in primates, we estimated the proportion of OR pseudogenes in 19 primate species by surveying randomly chosen subsets of 100 OR genes from each species. We find that apes, Old World monkeys and one New World monkey, the howler monkey, have a significantly higher proportion of OR pseudogenes than do other New World monkeys or the lemur (a prosimian). Strikingly, the howler monkey is also the only New World monkey to possess full trichromatic vision, along with Old World monkeys and apes. Our findings suggest that the deterioration of the olfactory repertoire occurred concomitant with the acquisition of full trichromatic color vision in primates.

Figure 1. Results of the Pilot Study in Human and Mouse

The percentage of OR genes from each family is given for the entire repertoire (filled bars) and a sample of 100 genes amplified using PC1 and PC2 degenerate primers (open bars). (A) OR genes in human. (B) OR genes in mouse. None of the differences between the full repertoires and the samples are significant at the 5% level. Only full-length OR genes (larger than 850 bp) were considered.

Figure 2. The Proportion of OR Pseudogenes in 20 Species

Primate species are color-coded according to family. The arrow points to the howler monkey. Datapoints (from left to right) are for apes (green): human (Homo sapiens), chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), orangutan (Pongo pygmaeus), gibbon (Hylobates syndactylus); for OWMs (blue): Guinea baboon (Papio papio), rhesus macaque (Macaca mulatta), silver langur (Trachypithecus auratus), mona (Cercopithecus mona), agile mangabey (Cercocebus agilis), black-and-white colobus (Colobus guereza); for NWMs (red): brown capuchin monkey (Cebus apella), southern owl monkey (Aotus azarai), spider monkey (Ateles fusciceps), black howler monkey (Alouatta caraya), squirrel monkey (Saimiri sciureus), wooly monkey (Lagothrix lagotricha), common marmoset (Callithrix jacchus); for one prosimian primate (brown): crowed lemur (Eulemur mongoz); and for the mouse (Mus musculus) (grey).

Figure 3. Phylogenetic Tree of Primates

Schematic phylogenetic tree of the primate species used in the current study. Phylogenetic relationships between species are based on Harada et al. (1995), Page et al. (1999), and Surridge et al. (2003). Arrows indicate on which lineages the acquisition of full trichromatic color vision occurred (Goodman et al. 1998; Jacobs and Deegan 2001). The red color highlights lineages with a high proportion of OR pseudogenes.