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

Yoav Gilad,Doron Lancet,Svante Pääbo,Molly Przeworski,Victor Wiebe,David Hillis David Hillis

doi:10.1371/journal.pbio.0020005

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.

Highlights

We find that a decrease in the size of the intact olfactory repertoire occurred independently in two evolutionary lineages: in the ancestor of Old World monkey (OWM) and apes, and in the New World howler monkey
2003), we found that the proportion of Olfactory receptor (OR) pseudogene in the great apes and rhesus macaque is approximately 30%
We further found that the proportion of OR pseudogenes in OWMs (29.3% 6 2.4%) is very similar to that of nonhuman apes (33.0% 6 0.8%), but notably higher than that of New World monkey (NWM)

Summary

Introduction

Olfactory receptor (OR) genes provide the basis for the sense of smell (Buck and Axel 1991) and, with more than 1,000 genes, comprise the largest gene superfamily in mammalian genomes (Glusman et al 2001; Zozulya et al 2001; Young andTrask 2002; Zhang and Firestein 2002; Olender et al 2003).OR genes are organized in clusters (Trask et al 1998; Young and Trask 2002) and in humans are found on every chromosome save the Y and 20 (Glusman et al 2001; Zozulya et al 2001). Genes could not be amplified by primers designed based on human sequences (Gilad et al 2003). We used two sets of degenerate primer pairs, constructed to amplify OR genes from all of the species studied (see Materials and Methods).

Results

Conclusion