Molecular evolution of the major chemosensory gene families in insects

Institut de Biologia Evolutiva (CSIC-UPF), Barcelona, Spain.
Heredity (Impact Factor: 3.81). 06/2009; 103(3):208-16. DOI: 10.1038/hdy.2009.55
Source: PubMed


Chemoreception is a crucial biological process that is essential for the survival of animals. In insects, olfaction allows the organism to recognise volatile cues that allow the detection of food, predators and mates, whereas the sense of taste commonly allows the discrimination of soluble stimulants that elicit feeding behaviours and can also initiate innate sexual and reproductive responses. The most important proteins involved in the recognition of chemical cues comprise moderately sized multigene families. These families include odorant-binding proteins (OBPs) and chemosensory proteins (CSPs), which are involved in peripheral olfactory processing, and the chemoreceptor superfamily formed by the olfactory receptor (OR) and gustatory receptor (GR) families. Here, we review some recent evolutionary genomic studies of chemosensory gene families using the data from fully sequenced insect genomes, especially from the 12 newly available Drosophila genomes. Overall, the results clearly support the birth-and-death model as the major mechanism of evolution in these gene families. Namely, new members arise by tandem gene duplication, progressively diverge in sequence and function, and can eventually be lost from the genome by a deletion or pseudogenisation event. Adaptive changes fostered by environmental shifts are also observed in the evolution of chemosensory families in insects and likely involve reproductive, ecological or behavioural traits. Consequently, the current size of these gene families is mainly a result of random gene gain and loss events. This dynamic process may represent a major source of genetic variation, providing opportunities for FUTURE specific adaptations.

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Available from: Julio Rozas, Apr 29, 2014
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    • "CSPs as well as OBPs could act in these processes as carriers of hormones and other regulatory compounds (Iovinella et al. 2013). Similar to insect olfactory receptors (ORs), OBPs were only found in Hexapoda, whereas CSP and gustatory receptor genes (GRs) have been identified in all major arthropod groups (Pelosi et al. 2006, 2014; Peñalva-Arana et al. 2009; Sanchez-Gracia et al. 2009; Smadja et al. 2009; Wanner et al. 2007; Wanner and Robertson 2008). This suggests that the OBP and OR gene families originated within the hexapodan lineage, whereas the CSP and GR families were already present in the last common ancestor of Hexapoda, Crustacea, and Chelicerata (~700 million years ago) (Hedges et al. 2006). "
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    ABSTRACT: Chemosensory protein (CSP) and gustatory receptor genes have been identified in all major arthropod groups. However, odorant binding proteins (OBP) and olfactory receptor genes are insect specific, suggesting that both gene families originated after the Hexapoda-Crustacea split (~470 million years ago). The seemingly parallel diversification of OBP and olfactory receptors has been suggested as coevolution between these genes after insect terrestrialization. To test this hypothesis we used the recently published transcriptomes of the jumping bristletail Lepismachilis y-signata and the firebrat Thermobia domestica to search for putative OBP and CSP sequences and analyzed their relationship to binding proteins of other insects and crustaceans. Our results suggest an evolution and expansion of OBPs as an adaptation to a terrestrial insect lifestyle, independently from the emergence of olfactory receptors.
    Chemical Senses 09/2015; DOI:10.1093/chemse/bjv050 · 3.16 Impact Factor
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    • "CSPs present in insects across different orders, including Diptera (4 CSPs in D. melanogaster, 8 CSPs in Anopheles gambiae [39]), Lepidoptera (10 CSPs in M. brassicae [28] and 16 CSPs in B. mori) and so on. Combining the recent discovery of 20 CSPs in Tribolium castaneum, these indicated the importance of CSPs and their potential as targets for pest control. "
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    ABSTRACT: Chemosensory proteins (CSPs) play important roles in chemical communication by insects, as they recognize and transport environmental chemical signals to receptors within sensilla. In this study, we identified HoblCSP1 and HoblCSP2 from a cDNA library of Holotrichia oblita antennae, successfully expressed them in E. coli and purified them by Ni ion affinity chromatography. We then measured the ligand-binding specificities of HoblCSP1 and HoblCSP2 to 50 selected ligands in a competitive binding assay. These results demonstrated that HoblCSP1 and HoblCSP2 have similar ligand-binding spectra. Both proteins displayed the highest affinity for β-ionone, α-ionone and cinnamaldehyde, indicating that they prefer binding to odorants other than sex pheromones. Additionally, immuno-localization revealed that HoblCSP1 is highly concentrated in sensilla basiconica, while HoblCSP2 is specifically localized to sensilla placodea. In conclusion, HoblCSP1 and HoblCSP2 are responsible for binding to general odorants with slightly different specificities due to their different in vivo environments.
    PLoS ONE 09/2014; 9(9):e107059. DOI:10.1371/journal.pone.0107059 · 3.23 Impact Factor
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    • "Some of the processes that have shaped the evolution of chemosensory gene sets have been extensively studied, albeit separately for each family and in different arthropod species or species sets (Robertson and Wanner 2006; Guo and Kim 2007; Vieira et al. 2007; Engsontia et al. 2008; Peñ alva-Arana et al. 2009; Smadja et al. 2009; Croset et al. 2010). These studies have revealed a few general patterns that have been summarized in a number of review papers (Nei et al. 2008; Sá nchez-Gracia et al. 2009). Overall, it has been shown that these families evolve according to the BD model, whereby new genes appear through duplication and are lost through deletion or pseudogenization (Nei and Hughes 1992; Nei and Rooney 2005). "
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    ABSTRACT: Gene turnover rates and the evolution of gene family sizes are important aspects of genome evolution. Here, we use curated sequence data of the major chemosensory gene families from Drosophila - the gustatory receptor (GR), odorant receptor (OR), ionotropic receptor (IR), and odorant binding protein (OBP) families - to conduct a comparative analysis among families, exploring different methods to estimate gene birth and death rates, including an ad hoc simulation study. Remarkably, we found that the state-of-the-art methods may produce very different rate estimates, which may lead to disparate conclusions regarding the evolution of chemosensory gene family sizes in Drosophila. Among biological factors, we found that a peculiarity of D. sechellia's gene turnover rates was a major source of bias in global estimates, whereas gene conversion had negligible effects for the families analyzed herein. Turnover rates vary considerably among families, subfamilies and ortholog groups, although all analyzed families were quite dynamic in terms of gene turnover. Computer simulations showed that the methods that use ortholog group information appear to be the most accurate for the Drosophila chemosensory families. Most importantly, these results reveal the potential of rate heterogeneity among lineages to severely bias some turnover rate estimation methods and the need of further evaluating the performance of these methods in a more diverse sampling of gene families and phylogenetic contexts. Using branch-specific codon substitution models, we find further evidence of positive selection in recently duplicated genes, which attests to a non-neutral aspect of the gene birth-and-death process.
    Genome Biology and Evolution 06/2014; 6(7). DOI:10.1093/gbe/evu130 · 4.23 Impact Factor
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