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The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity

Key Points

  • Chemosensory receptors recognize chemical signals of odorants and tastants in the environment. Six multigene families are known to encode chemosensory receptors in vertebrates and two multigene families in insects, respectively.

  • Near-complete repertoires of chemosensory receptor genes have been determined from the genomic sequences of various organisms. These studies have shown that the number of chemosensory receptor genes is generally large and varies greatly among different organisms.

  • A substantial portion of interspecific variation in gene number can be explained by adaptation to different environments. There was a large increase in the number of olfactory receptor genes when fishes evolved into land animals that needed to detect airborne odorants, but this number decreased drastically when mammals adapted to aquatic life.

  • Vertebrate species have many chemosensory receptor pseudogenes as well as functional genes. There is no clear relationship between the number of pseudogenes and environmental changes.

  • Genomic drift, a random process of gene duplication and deletion, has generated a large amount of gene copy-number variation among individuals of the same species. The number of odorant receptor genes and pseudogenes both followed a normal distribution in human populations.

  • The similarity in the distribution of functional genes to the distribution of pseudogenes suggests that the copy-number variation of functional genes is almost neutral.

  • The number of chemosensory receptor genes is generally much smaller in insects than in vertebrates. The proportion of pseudogenes is also smaller in insects.

Abstract

Chemosensory receptors are essential for the survival of organisms that range from bacteria to mammals. Recent studies have shown that the numbers of functional chemosensory receptor genes and pseudogenes vary enormously among the genomes of different animal species. Although much of the variation can be explained by the adaptation of organisms to different environments, it has become clear that a substantial portion is generated by genomic drift, a random process of gene duplication and deletion. Genomic drift also generates a substantial amount of copy-number variation in chemosensory receptor genes within species. It seems that mutation by gene duplication and inactivation has important roles in both the adaptive and non-adaptive evolution of chemosensation.

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Figure 1: Chemosensory receptors and their genes.
Figure 2: Numbers of chemosensory receptor genes in vertebrates and insects.
Figure 3: Distribution of chemosensory receptor genes in the human genome.
Figure 4: Evolutionary dynamics of olfactory receptor genes.
Figure 5: Copy-number variation and genomic drift.

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Acknowledgements

We thank Y. Go for providing unpublished data. This work was supported by National Institutes of Health grant GM020293 to M.N. and Japanese Government Grants 17710162 and 20770192 to Y.N.

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Glossary

Chemosensation

The sense of smell and taste.

Multigene family

A group of genes that have descended from a common ancestor, and therefore have similar functions and similar DNA sequences.

Pheromone

A chemical substance that is released and detected by different individuals of the same species, and triggers physiological and behavioural responses.

Main olfactory epithelium

A specialized epithelial tissue in the nasal cavity in which olfactory receptor genes are expressed.

Ectopic expression

The expression of a gene in tissues other than the tissue in which it is normally expressed.

Vomeronasal organ

An auxiliary olfactory organ that is found in many mammals, reptiles and amphibians.

Proboscis

The tubular organ in insects that is used for feeding and sucking.

Non-synonymous nucleotide substitution

A nucleotide substitution that results in a change of an amino acid within the coding region of a gene.

Synonymous nucleotide substitution

A nucleotide substitution that does not change an amino acid in the coding region of a gene.

Electroreception

The ability of an animal to perceive electrical pulses.

Mechanoreception

The ability of an animal to detect certain kinds of stimuli, such as touch, sound and changes in atmospheric pressure or posture in its environment.

Toothed whales

A suborder of cetaceans that have teeth rather than baleens (plates of whalebone). Toothed whales include dolphins, sperm whales, beaked whales and killer whales.

Echolocation

A biological sonar mechanism used by several mammals, such as whales and bats. A high-pitched sound (usually clicks) is sent out by an animal, the sound bounces off an object and some of the sound returns to the animal. Whales perceive this returning echo to determine the shape, direction, distance and texture of the object.

Birth-and-death evolution

An evolutionary mechanism that occurs in multigene families, in which new genes are created by gene duplication and some are retained in the genome for a long time as functional genes, but other genes are inactivated or eliminated from the genome.

Genetic drift

The random change of the allele frequency in populations.

Hitch-hiking

The increase in the frequency of a neutral allele at a locus that is physically linked to an advantageous allele at a different locus.

Overdominant selection

A form of selection caused by heterozygote advantage.

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Nei, M., Niimura, Y. & Nozawa, M. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9, 951–963 (2008). https://doi.org/10.1038/nrg2480

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