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Molecular evolution of the major chemosensory gene families in insects

Institut de Biologia Evolutiva (CSIC-UPF), Barcelona, Spain.
Heredity (Impact Factor: 3.8). 06/2009; 103(3):208-16. DOI: 10.1038/hdy.2009.55
Source: PubMed

ABSTRACT 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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    • "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 · 4.53 Impact Factor
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    • "This means that there are more gene duplications and losses in CSP gene family than in gene families on average. Rapid turnover rates have been observed in other chemosensory gene families of many insects (Vieira et al., 2007; Gardiner et al., 2008; Zhou et al., 2010) and the rate of turnover in CSP gene family falls well within the turnover rates estimated for Drosophila in OBP (l ¼ 0.005), OR (l ¼ 0.006) and GR (l ¼ 0.011) gene families (Sánchez-Gracia et al., 2009, estimated with program CAFE). "
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    ABSTRACT: Gene duplications can have a major role in adaptation, and gene families underlying chemosensation are particularly interesting due to their essential role in chemical recognition of mates, predators and food resources. Social insects add yet another dimension to the study of chemosensory genomics, as the key components of their social life rely on chemical communication. Still, chemosensory gene families are little studied in social insects. Here we annotated chemosensory protein (CSP) genes from seven ant genomes and studied their evolution. The number of functional CSP genes ranges from 11 to 21 depending on species, and the estimated rates of gene birth and death indicate high turnover of genes. Ant CSP genes include seven conservative orthologous groups present in all the ants, and a group of genes that has expanded independently in different ant lineages. Interestingly, the expanded group of genes has a differing mode of evolution from the orthologous groups. The expanded group shows rapid evolution as indicated by a high dN/dS (nonsynonymous to synonymous changes) ratio, several sites under positive selection and many pseudogenes, whereas the genes in the seven orthologous groups evolve slowly under purifying selection and include only one pseudogene. These results show that adaptive changes have played a role in ant CSP evolution. The expanded group of ant-specific genes is phylogenetically close to a conservative orthologous group CSP7, which includes genes known to be involved in ant nestmate recognition, raising an interesting possibility that the expanded CSPs function in ant chemical communication.Heredity advance online publication, 13 February 2013; doi:10.1038/hdy.2012.122.
    Heredity 02/2013; 110(6). DOI:10.1038/hdy.2012.122 · 3.80 Impact Factor
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    • "In addition, sequencing of limited number of randomly selected cDNA clones often have insufficient coverage of less abundant transcripts [15]. Among the available insect olfactory genes, the majority of them have been obtained by means of bioinformatic approaches based on the characteristic features of the protein families from the completed genome sequences [9] [16]. Over the past several years, the next generation sequencing technology has emerged as a cutting edge approach for high-throughput sequence determination, promptly improved the efficiency and speed of gene discover, and provided fascinating opportunities in the life sciences with dramatically reduced time, labor, and cost in nonmodel organisms [17] [18] [19]. "
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    ABSTRACT: The most important proteins involved in olfaction include odorant binding protein (OBP), chemosensory protein (CSP), olfactory receptor (OR), and gustatory receptor (GR). Despite that the exhaustive genomic analysis has revealed a large number of olfactory genes in a number of model insects, it is still poorly understood for most nonmodel species. This is mostly due to the reason that the small antenna is challenging for collection. We can generally isolate one or few genes at a time by means of the traditional method. Here, we present the large-scale identifying members of the main olfactory genes from the head of Tomicus yunnanensis using Illumina sequencing. In a single run, we obtained over 51.8 million raw reads. These reads were assembled into 57,142 unigenes. Nearly 29,384 of them were functionally annotated in the NCBI nonredundant database. By depth analysis of the data, 11 OBPs, 8 CSPs, 18 ORs, and 8 GRs were retrieved. Sequences encoding full length proteins were further characterised for one OBP and two CSPs. The obtained olfactory genes provide a major resource in further unraveling the molecular mechanisms of T. yunnanensis chemoperception. This study indicates that the next generation sequencing is an attractive approach for efficient identification of olfactory genes from insects, for which the genome sequence is unavailable.
    Comparative and Functional Genomics 06/2012; 2012:491748. DOI:10.1155/2012/491748 · 1.75 Impact Factor
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