Olfactory Receptor Genes: Evolution


Many mammal genomes have approximately 1000 genes encoding olfactory receptors (ORs), and OR genes constitute the largest multigene family in mammals. Comparisons among the OR gene repertoires in a broad range of species demonstrates that gene duplication and pseudogenization cause frequent gene gain and loss in this family, causing drastic evolutionary changes in the number of genes depending on species' ecological niches and other sensory modalities. For example, higher primates are equipped with a well‐developed visual system, and they have a reduced OR gene repertoires relative to mammals with lesser visual systems. Additionally, aquatic and terrestrial vertebrates retain different sets of OR genes, and these sets reflect the capacity to detect water‐soluble and airborne odorants, respectively. The origin of vertebrate OR genes can be traced back to the common ancestor of chordates, but insects and nematodes each use a distinct family of genes to encode chemoreceptors; therefore, multiple distinct chemoreceptor gene families emerged independently during animal evolution.

Key Concepts:

  • Olfactory receptor (OR) genes are the largest multigene family in mammals.

  • OR gene repertoires changed dynamically during mammalian evolution and these changes depended on each species' ecological niches and other sensory modalities.

  • Distinct chemoreceptor gene families have emerged independently multiple times during animal evolution.

  • Comparative evolutionary analysis of OR genes provides insights into the interactions between genomes and environments.

Keywords: olfactory receptor; chemoreceptor; phylogenetic analysis; multigene family; birth‐and‐death evolution; G‐protein coupled receptor; chordates; vertebrates; mammals; primates

Figure 1.

Complexity of structure–odour relationships (Rossiter, ). (a) The molecule on the left conveys a strong ambergris odour, but molecule on the right is odourless because it lacks just one of the oxygen atoms. (b) Enantiomers that have different odours. (c) Five very different molecular structures all have musky odours. (d) Four very different molecular structures all have camphoraceous odours, though there is no one functional group that is common to each of them.

Figure 2.

Number of OR genes identified from the whole genome sequences of 30 chordate species. Each number in the bar graphs indicates the number of intact genes (red), truncated genes (yellow) or pseudogenes (dark blue). For zebra finch and two turtle species, no distinction was made between truncated genes and pseudogenes. ‘P%’ indicates the fraction of pseudogenes. Data from Niimura and Nei (), Niimura (), Matsui et al. () and Wang et al. ().

Figure 3.

OR genes in the human genome. (a) Vertical bars above and below the chromosomes represent locations of intact OR genes and OR pseudogenes, respectively. The height of each bar indicates the number of OR genes existing in a nonoverlapping 1‐Mb window. (b) The OR gene cluster indicated by the red arrow in (a). The diagram (left) represents an expanded view of a 0.6‐Mb region on chromosome 3. ‘Ψ’ represents a pseudogene. All genes are encoded on the same strand. The neighbor‐joining phylogenetic tree (right) for the genes contained in this 0.6‐Mb cluster indicates that neighbouring genes within the cluster tend to be more closely related to each other than to more distantly located genes within the cluster. For example, genes 16 and 17 are more closely related to each other than they are to the other genes. HsOR11.3.2 was used as the outgroup in the phylogenetic tree. Bootstrap values greater than 80% are shown. (a) and (b) were modified from Nei et al. (). © Nature Publishing Group. (c) Schematic representation of tandem gene duplication. Unequal crossing‐over generates a new gene copy (‘B’) adjacent to the original gene. Subsequently, independent accumulation of mutations causes the sequences of the duplicates to diverge and potentially to acquire distinctive functions (‘B1’ and ‘B2’).

Figure 4.

Evolutionary dynamics of OR genes in primates (a) and in mammals (b). (a) OR gene losses during primate evolution. The common ancestor of the five primate species is estimated to have had 551 functional OR genes. The number above each branch indicates the number of the ancestral OR genes that were lost in that lineage. For example, humans have lost 212 of the 551 putative ancestral OR genes, but 57 gene duplications apparently occurred; therefore, humans currently have 396 functional OR genes. An arrowhead with red and green represents the branch at which the duplication of red/green opsin genes occurred. Colour vision system in each species is also shown (right). X‐linked red/green opsin genes and an autosomal blue opsin gene are represented schematically. Modified with permission from Matsui et al. (). © Oxford University Press. (b) Gains and losses of OR genes during mammalian evolution. The number in each box indicates the number of functional OR genes in the indicated extant species or ancestral species. The numbers with a plus or minus sign indicate estimated numbers of gene gains and losses, respectively, along each branch. Modified from Niimura and Nei (). © PLoS One.

Figure 5.

Evolution of OR genes in vertebrates. (a) Neighbour‐joining phylogenetic tree constructed by using all intact OR genes identified from amphioxus, lamprey, zebrafish, and human. Several non‐OR GPCR genes were used as the outgroup. Bootstrap values are shown for major clades. Modified from Niimura (). © Oxford University Press. (b) Number of intact OR genes in each gene group for each species. The volume of a sphere is proportional to the number of genes in the group. Terrestrial‐type and aquatic‐type OR genes are represented by red and blue, respectively. Data from Niimura () and Wang et al. ().



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Further Reading

Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444: 295–301.

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Niimura, Yoshihito(Aug 2014) Olfactory Receptor Genes: Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020789.pub2]