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 and Trask 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). On the basis of sequence similarity, they are classified into two major classes and 17 families (Glusman et al. 2001). All OR genes have an approximately 1 kb coding region that is uninterrupted by introns (Ben-Arie et al. 1994; Gilad et al. 2000).
approximately 60% of human OR genes carry one or more coding region
disruptions and are therefore considered pseudogenes (Rouquier et al. 1998; Glusman et al. 2001; Zozulya et al. 2001). In nonhuman apes, the fraction of OR pseudogenes is only approximately 30% (Gilad et al. 2003).
However, both humans and other apes have a significantly higher
fraction of OR pseudogenes than do the mouse or the dog (approximately
20%) (Young et al. 2002; Zhang and Firestein 2002; Olender et al. 2003).
Thus, there has been a decrease in the size of the intact OR repertoire
in apes relative to other mammals, with a further deterioration in
humans (Rouquier et al. 2000; Gilad et al. 2003).
the causes are unclear, it seems reasonable to speculate that the high
fraction of OR pseudogenes in apes reflects a decreased reliance on the
sense of smell in species for whom auditory and visual cues may be more
important (e.g., Dominy and Lucas 2001).
We were therefore interested in investigating whether the high fraction
of OR pseudogenes is characteristic of primates as a whole and, if not,
to pinpoint when the proportion of OR pseudogenes increased. To this
end, we randomly selected subsets of 100 OR genes in 19 primate
species, including a human, four apes, six Old World monkeys (OWMs),
seven New World monkeys (NWMs) and one prosimian. We find that a
decrease in the size of the intact olfactory repertoire occurred
independently in two evolutionary lineages: in the ancestor of OWMs and
apes, and in the New World howler monkey.