Research Article: Loss of Olfactory Receptor Genes Coincides with the Acquisition of Full Trichromatic Vision in Primates

Date Published: January 20, 2004

Publisher: Public Library of Science

Author(s): Yoav Gilad, Victor Wiebe, Molly Przeworski, Doron Lancet, Svante Pääbo

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.

Partial Text: 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).

Owing to the high levels of DNA sequence divergence among the primate species in our sample, orthologous OR genes could not be amplified by primers designed based on human sequences (Gilad et al. 2003). Instead, we used two sets of degenerate primer pairs, constructed to amplify OR genes from all of the species studied (see Materials and Methods). We then cloned the PCR products and determined the sequences of clones until we had identified 100 distinct OR genes from each species. A danger of this approach is that degenerate primers may bind preferentially to certain OR genes, thereby resulting in a biased representation of the OR repertoire. To safeguard against this, we tested the degenerate primers on human and mouse, for which the entire OR gene repertoire is known, by using them to amplify 100 OR genes from the two species. The sample thus obtained faithfully represented the composition of the full OR gene repertoire in human and mouse with respect to the 17 OR gene families (Figure 1). Moreover, the sample estimates of the fractions of pseudogenes were accurate (see Materials and Methods; Figure 2). This pilot study demonstrates that the degenerate primers yield an unbiased representation of the OR gene repertoire, as measured by the family composition and pseudogene content of the human and mouse samples. Since the primers performed well both in human and a distantly related species, the mouse, there was no reason to assume that they would not do so in nonhuman primate species.



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