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.

Download full-text


Available from: Julio Rozas, Apr 29, 2014
    • "Odorant receptors represent valuable targets since they ensure the direct interaction with odor ligands, eliciting signal transduction mechanisms that will ultimately lead to specific behaviors (Touhara and Vosshall, 2009) (Carey and Carlson, 2011) (Leal, 2013). In addition, insect ORs have been shown to undergo rapid evolution (Robertson et al., 2003) (Sanchez-Gracia et al., 2009), which is consistent with a role in the adaptation to different ecological environments. A search of the genome data revealed eight full-length putative OR genes, confirming the limited range of this family in this insect. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The body louse, Pediculus humanus humanus, is an obligate blood-feeding ectoparasite and an important insect vector that mediates the transmission of diseases to humans. The analysis of the body louse genome revealed a drastic reduction of the chemosensory gene repertoires when compared to other insects, suggesting specific olfactory adaptations to host specialization and permanent parasitic lifestyle. Here, we present for the first time functional evidence for the role of odorant receptors (ORs) in this insect, with the objective to gain insight into the chemical ecology of this vector. We identified seven putative full-length ORs, in addition to the odorant receptor co-receptor (Orco), and expressed four of them in the Xenopus laevis oocytes system. When screened with a panel of ecologically-relevant odorants, PhumOR2 responded to a narrow set of compounds. At the behavior level, both head and body lice were repelled by the physiologically-active chemicals. This study presents the first evidence of the OR pathway being functional in lice and identifies PhumOR2 as a sensitive receptor of natural repellents that could be used to develop novel efficient molecules to control these insects.
    Insect biochemistry and molecular biology 10/2015; 66. DOI:10.1016/j.ibmb.2015.10.009 · 3.45 Impact Factor
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    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
Show more