Comparative Genomics of the Major Chemosensory Gene Families in Arthropods

Abstract

Chemoreception is the most important sense for the survival and reproduction of most animal species. In insects, the principal proteins involved in the recognition of chemical cues comprise moderately sized, multigene families. These families include (i) odorant‐binding (OBPs) and chemosensory (CSPs) proteins, which are involved in peripheral olfactory processing; (ii) the chemoreceptor super‐family, formed by the olfactory (OR) and gustatory (GR) receptors; and (iii) the ionotropic receptors (IR), a variant class of ionotropic glutamate receptors (iGluR). Recent comparative genomic analyses of fully sequenced arthropod genomes support the birth‐and‐death model as the major evolutionary mechanism in determining the chemosensory repertoire size, and provide evidence of adaptive changes fostered by ecological shifts that might influence the current size of chemosensory families. These studies also advocate for the origin of olfactory gene families with the evolution of terrestriality in insects.

Key Concepts:

  • The chemosensory system mediates the detection of food, predators and mates, eliciting feeding behaviours and innate sexual and reproductive responses.

  • In arthropods, the most important proteins involved in the recognition of chemical cues comprise moderately sized multigene families.

  • The chemosensory system of arthropods relies on transmembrane receptors (OR, GR and IR gene families) and small globular proteins (OBP and CSP families).

  • The number of chemosensory genes is similar across the Drosophila genus, with little variation in the gene number among species.

  • New OBP and CSP genes appear by gene duplication in extant chromosomal clusters, and diverge independently from each other.

  • An unexpectedly high number of gene gains and losses occurred in the evolution of chemosensory families during the 40–60 Myr of divergence of the Drosophila genus.

  • The chemosensory families in insects evolve under a birth‐and‐death process, with lineage‐specific family size expansions and contractions at large time scale.

  • The selective constraints on chemosensory genes have varied over the evolution of the Drosophila genus, with some cases of positive selection.

  • Random genomic drift, assisted by eventual adaptation processes, is the principal determinant of the chemosensory family size of arthropods.

Keywords: chemosensory system; multigene families; odorant‐binding proteins; odorant receptors; gustatory receptors; ionotropic receptors; family size; birth‐and‐death model; positive selection

Figure 1.

Phylogenetic relationships of the insect OBP proteins. The phylogenetic tree includes sequences from Drosophila melanogaster and Drosophila mojavensis (red branches), Anopheles gambiae (blue branches), Bombyx mori (brown branches), Tribolium castaneum (green branches), Apis mellifera (orange branches), Pediculus humanus (pink branches) and Acyrthosyphon pisum (cyan branches). The coloured ring represents the phylogenetic subfamilies (Classic OBPs in black, Minus‐C in green, Plus‐C in blue, Dimer in red, D7 in yellow, ABPI in cyan, ABPII in grey and PBP/GOBP in pink). The scale bar represents one amino acid substitution per site.

Figure 2.

Phylogenetic relationships of the receptor superfamily in a group of arthropod species. The phylogenetic tree includes GR sequences from Drosophila melanogaster (red branches), Anopheles gambiae (blue branches), Daphnia pulex (green branches) and Ixodes scapularis (magenta branches) and some representatives of the OR family from insects (yellow branches). The putative carbon dioxide and sugar receptors in these species are indicated between dashed lines.

Figure 3.

Phylogenetic relationships of IR genes form Drosophila melanogaster (red branches) and Anopheles gambiae (blue branches) genomes. Names in green designate the IR genes with antennal expression. Yellow shaded lineages correspond to the iGluR subgroup members. The scale bar represents 0.8 amino acid substitutions per site.

Figure 4.

Estimates of the number of OBP and IR genes (pseudogenes are indicated in parenthesis) on terminal branches and internal nodes of the Drosophila genus phylogeny are coloured in red. The number of gene gains (on the branch), gene losses and pseudogenisation events (indicated in parentesis) are indicated with black numbers on each branch. Data from Vieira et al. and Croset et al..

Figure 5.

Notch plots of the ω values (dN/dS rates) estimated for each chemosensory family in the melanogaster group of Drosophila. Ant_IR, IR genes with antennal expression.

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Sánchez‐Gracia, Alejandro, Vieira, Filipe G, Almeida, Francisca C, and Rozas, Julio(Feb 2011) Comparative Genomics of the Major Chemosensory Gene Families in Arthropods. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022848]