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Comparative Study
. 2018 Apr 1;10(5):1221-1236.
doi: 10.1093/gbe/evy081.

Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates

Joel Vizueta  1 , Julio Rozas  1 , Alejandro Sánchez-Gracia  1
Affiliations
Comparative Study

Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates

Joel Vizueta et al. Genome Biol Evol. .

Abstract

Chemoreception is a widespread biological function that is essential for the survival, reproduction, and social communication of animals. Though the molecular mechanisms underlying chemoreception are relatively well known in insects, they are poorly studied in the other major arthropod lineages. Current availability of a number of chelicerate genomes constitutes a great opportunity to better characterize gene families involved in this important function in a lineage that emerged and colonized land independently of insects. At the same time, that offers new opportunities and challenges for the study of this interesting animal branch in many translational research areas. Here, we have performed a comprehensive comparative genomics study that explicitly considers the high fragmentation of available draft genomes and that for the first time included complete genome data that cover most of the chelicerate diversity. Our exhaustive searches exposed thousands of previously uncharacterized chemosensory sequences, most of them encoding members of the gustatory and ionotropic receptor families. The phylogenetic and gene turnover analyses of these sequences indicated that the whole-genome duplication events proposed for this subphylum would not explain the differences in the number of chemoreceptors observed across species. A constant and prolonged gene birth and death process, altered by episodic bursts of gene duplication yielding lineage-specific expansions, has contributed significantly to the extant chemosensory diversity in this group of animals. This study also provides valuable insights into the origin and functional diversification of other relevant chemosensory gene families different from receptors, such as odorant-binding proteins and other related molecules.

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Figures

<sc>Fig</sc>. 1.—
Fig. 1.—
Phylogenetic relationships among the 14 surveyed species. Divergence times are given in millions of years. Some branches representative of major lineages are shaded in different colors. Green, insects; light blue, crustaceans; dark blue, myriapods; black, horseshoe crabs; orange, acari; brown, scorpions; red, spiders. Numbers in the right part of the figure indicate the number of CS encoding sequences separated per each family (SMIN values).
<sc>Fig</sc>. 2.—
Fig. 2.—
Workflow showing the steps used for the identification and annotation of the chemosensory gene families.
<sc>Fig</sc>. 3.—
Fig. 3.—
Phylogenetic tree of the Gr family members across arthropods. The different species are depicted in colors as in figure 1. The scale bar represents one amino acid substitutions per site.
<sc>Fig</sc>. 4.—
Fig. 4.—
Phylogenetic tree of the Ir/iGluR family members across arthropods. The tree is based on LCD domain sequences (PF00060). Different lineages are colored as in figure 1. The three main subfamilies of iGluRs and the conserved IR clade are shaded in different colors. The scale bar represents one amino acid substitution per site.
<sc>Fig</sc>. 5.—
Fig. 5.—
Phylogenetic relationships of the Obp-like and insect (D. melanogaster) Obp family members. Lineages and species names are colored as in figure 1. For clarity, two D. melanogaster nodes with 12 and 33 descent sequences are collapsed. The color of the inner circle indicates the Obp subfamily: Classic (black), Minus-C (green), Plus-C (blue) and Dimer (red). The outer circle in yellow indicates the members from noninsect species with PBP/GOBP domain (IPR006170). The scale bar represents 0.1 amino acid substitutions per site.
<sc>Fig</sc>. 6.—
Fig. 6.—
Gene turnover of chemoreceptors across chelicerates. Estimates obtained from the data set used to estimate SMIN. Numbers above and below each branch indicate lineage-specific gene duplications and losses, respectively. Green, GR family; blue, IR/iGluR family. Estimates in very short and outgroup branches have large uncertainty and are not showed. Numbers in the ancestral nodes show the estimated family sizes. Numbers at the tips indicate the number of sequences used for the analysis; such values can differ from SMIN because only sequences that clustered in an orthogroup (with three or more sequences) were included in the analysis.
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