Unusual Pattern of Nucleotide Sequence Variation at the OS-E and OS-F Genomic Regions of Drosophila simulans

Abstract

Nucleotide variation at the genomic region encompassing the odorant-binding protein genes OS-E and OS-F (OS region) was surveyed in two populations of Drosophila simulans, one from Europe and the other from Africa. We found that the European population shows an atypical and large haplotype structure, which extends throughout the $5-kb surveyed genomic region. This structure is depicted by two major haplotype groups segregating at intermediate frequency in the sample, one haplogroup with nearly no variation, and the other at levels more typical for this species. This pattern of variation was incompatible with neutral predictions for a population at a stationary equilibrium. Nevertheless, neutrality tests contrasting polymorphism and divergence data fail to detect any departure from the standard neutral model in this species, whereas they confirm the non-neutral behavior previously observed at the OS-E gene in D. melanogaster. Although positive Darwinian selection may have been responsible for the observed unusual nucleotide variation structure, coalescent simulation results do not allow rejecting the hypothesis that the pattern was generated by a recent bottleneck in the history of European populations of D. simulans. SMELL is one of the oldest and most important senses of animals. Olfaction allows for the recognition and discrimination of the chemical signals that provide animals the essential information needed to detect and assess food, to identify mating partners and predators, and to adopt individual and collective behavior. Positive natural selection can therefore play a major role in the evolution of olfactory system genes; indeed, human olfaction-involved genes are among the most fast-evolving genes (e.g., Clark et al. 2003;Gilad et al. 2003;Nielsen et al. 2005; see also Gimelbrant et al. 2004). Furthermore, Darwinian positive selection has been proposed to be driving the evolution of some olfactory system genes in rodents (Emes et al. 2004), channel catfish (Ngai et al. 1993), salamander (Watts et al. 2004Palmer et al. 2005), and insects (Willett 2000; Ross 2002, 2005).The olfactory system constitutes the principal sensory modality of invertebrates, showing a high specificity and sensitivity. Odorant receptors (OR) are located in the external membrane of specialized sensory neurons, which extend their dendrites into an aqueous fluid. Hydrophobic odors traverse the fluid space bound to odorant-binding proteins (OBPs), which deliver them close to receptors. The OBP multigene family includes two different subfamilies of proteins: the general odorant-binding proteins, which bind and transport general odorants, and the pheromone-binding proteins, which specialize in pheromone perception (Vogt and Riddiford 1981;Pelosi and Maida 1995). Phylogenetic analysis indicates that these OBPs show a monophyletic origin (Vogt et al. 1999;Hekmat-Scafe et al. 2000). There is little knowledge about the evolution of the Drosophila OBP multigene family. This family contains 51 putative members located in clusters an...

Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birth-and-death evolution

“…We found that OBP genes exhibit high functional constraints, with an average ω value of 0.153, and confirmed that the results obtained in two individual members are a general feature of the family [ 63 , 64 ]. In spite of the fact that the selective constraint levels are not clearly associated with phylogenetic groups, they differ both among individual genes and across chromosome clusters.…”

Molecular population genetics of the OBP83 genomic region in Drosophila subobscura and D. guanche: contrasting the effects of natural selection and gene arrangement expansion in the patterns of nucleotide variation

“…Estimates of silent nucleotide diversity in the Obp83 region of D. subobscura are higher than those determined in European populations of D. melanogaster and D. simulans (Sánchez-Gracia et al, 2003;Sánchez-Gracia and Rozas, 2007). This high level of DNA variation allowed us to conduct a fine analysis of the functional constraints along the Obp83 region.…”

“…Figure 3 shows the distribution of silent nucleotide polymorphisms and divergence throughout the Obp83 region. As in D. melanogaster and D. simulans (Sánchez-Gracia et al, 2003;Sánchez-Gracia and Rozas, 2007), the level of silent variation is lower in the Obp83a gene than in Obp83b and intergenic regions (except for a highly variable B300-bp fragment in the first intron of the Obp83a gene). Nevertheless, the HKA test does not reject the hypothesis that polymorphism and divergence are correlated, as expected under the neutral model (HKA test, results not shown).…”

A Large Panel of Drosophila simulans Reveals an Abundance of Common Variants

“…2001 ; Quesada et al. 2003 ; Sanchez-Gracia and Rozas 2007 ). In general, our results are suggestive of a contribution of both demography and selection to the patterns of variation observed in D. simulans .…”