Molecular evolution of the major chemosensory gene families in insects

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.

Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

“…Our findings on CSP gene family evolution in ants agree with reports on highly dynamic evolution of animal chemosensory genes by birthand-death model (Nei et al, 2008;Sánchez-Gracia et al, 2009), but depart from those studies that found insect CSPs to be a conserved gene family (Sánchez-Gracia et al, 2009). Earlier studies have shown that many insect CSPs are ancient and shared by different insect orders Gong et al, 2007;Xu et al, 2009).…”

“…The number of gene copies within a gene family can vary extensively between species and even within a species (Schrider and Hahn, 2010). This copy number variation has been suggested to have a significant role in adaptation and could provide raw material for genes with new functions (Sánchez-Gracia et al, 2009;Innan and Kondrashov, 2010). Rapid turnover of genes within a gene family has been shown to correlate with fast evolution at sequence level (Chen et al, 2010), and gene families which are conserved in size also evolve, on average, more slowly at sequence level.…”

“…OBPs and CSPs belong to different gene families, but possibly have common evolutionary origin of 380-450 million years ago (Mya) . Several studies find that chemosensory gene families evolve under purifying selection and there is no or little indication of positive selection Vieira et al, 2007;Gardiner et al, 2008;Sánchez-Gracia et al, 2009;Zhou et al, 2010). Exceptions are the pea aphid OR and GR gene families, where the most recent expansions evolve under positive selection (Smadja et al, 2009) with ecologically based selection for host plant specialization as the possible driving force.…”

“…Among these are genes involved in immune defense, stress response, metabolism, cell signaling, reproduction and chemoreception (Demuth and Hahn, 2009). Genes underlying chemosensation have been studied in several insects (Nozawa and Nei, 2007;Vieira et al, 2007;Sánchez-Gracia et al, 2009;Smadja et al, 2009;Zhou et al, 2010;Vieira and Rozas, 2011). Within chemosensory gene families, relatively few genes can be recognized as orthologues shared by different insect orders, and the number of orthologous groups quickly decreases with increasing divergence time .…”

Comparing the Expression of Olfaction-Related Genes in Gypsy Moth (Lymantria dispar) Adult Females and Larvae from One Flightless and Two Flight-Capable Populations

“…ORs are expressed in the cell membranes of olfactory sensory neurons (OSNs) and are responsible for the detection of odor molecules (Sanchez-Gracia et al, 2009). In general, OSNs will express either ORs or IRs, with the latter mostly tuned to compounds of lower molecular weight (Hallem et al, 2004(Hallem et al, , 2006Benton et al, 2009;Silbering et al, 2011).…”