Evolutionary dynamics of olfactory receptor genes in chordates: interaction between environments and genomic contents

Abstract

Olfaction is essential for the survival of animals. Versatile odour molecules in the environment are received by olfactory receptors (ORs), which form the largest multigene family in vertebrates. Identification of the entire repertories of OR genes using bioinformatics methods from the whole-genome sequences of diverse organisms revealed that the numbers of OR genes vary enormously, ranging from approximately 1,200 in rats and approximately 400 in humans to approximately 150 in zebrafish and approximately 15 in pufferfish. Most species have a considerable fraction of pseudogenes. Extensive phylogenetic analyses have suggested that the numbers of gene gains and losses are extremely large in the OR gene family, which is a striking example of the birth-and-death evolution. It appears that OR gene repertoires change dynamically, depending on each organism's living environment. For example, higher primates equipped with a well-developed vision system have lost a large number of OR genes. Moreover, two groups of OR genes for detecting airborne odorants greatly expanded after the time of terrestrial adaption in the tetrapod lineage, whereas fishes retain diverse repertoires of genes that were present in aquatic ancestral species. The origin of vertebrate OR genes can be traced back to the common ancestor of all chordate species, but insects, nematodes and echinoderms utilise distinctive families of chemoreceptors, suggesting that chemoreceptor genes have evolved many times independently in animal evolution.

Figure 1

Numbers of OR genes in 23 chordate species[12-14]. F, T and P indicate the numbers of functional genes, truncated genes and pseudogenes, respectively. A truncated gene is part of an intact sequence that is located at a contig end. The fraction of pseudogenes (P per cent) in each species was estimated by assuming that all truncated genes are functional[12]. Phylogenetic relationships among the 23 species are also shown.

Figure 2

Evolutionary changes in the number of olfactory receptor (OR) genes in mammals. (a) Estimated numbers of functional OR genes (red) and OR pseudogenes (blue) in the most recent common ancestor (MRCA) between humans and chimpanzees. The numbers in humans and chimpanzees are also shown. 'F →F' ('P → P') indicates that a functional gene (a pseudogene) in the MRCA is still functional (a pseudogene) in humans or chimpanzees. 'F → P' represents a functional gene in the MRCA becoming a pseudogene in the human or chimpanzee lineage. A grey triangular area depicts deletion from the genome; for example, 62 pseudogenes in the MRCA were eliminated from the human genome. Adapted from Go and Niimura (2008)[13]. (b) Gains and losses of OR genes in mammalian evolution. A number in a box represents the number of functional OR genes in the extant or ancestral species. A number with a plus and a minus sign indicates the number of gene gains and losses, respectively, for each branch. Adapted from Niimura and Nei (2007).[12]

Figure 3

(a) Neighbour-joining phylogenetic tree containing all functional olfactory receptors (OR) genes in the amphioxus, lamprey, zebrafish and human. Non-OR G-protein coupled receptor (GPCR) genes were used as the outgroup. The Type 2 clade contains several non-OR genes that are not included in group η[14]. Bootstrap values obtained from 500 resamplings are shown for major clades. A scale bar represents the estimated number of amino acid substitutions per site. Adapted from Niimura (2009)[14]. (b) Numbers of functional OR genes (including truncated genes) belonging to groups α - η in teleost fish and tetrapods.[14]

Figure 4

The evolutionary scenario of OR genes in chordates[14,37]. Phylogenetic analyses suggested that the divergence between type 1 (circles) and type 2 (triangles) occurred before the divergence between jawless and jawed vertebrates, and the divergence among groups α - ζ (circles in different colours) predate the divergence between teleost fish and tetrapods. In terrestrial organisms, group α (red circles) and γ genes (blue circles) have largely expanded.