A reanalysis of protein polymorphism in Drosophila melanogaster, D. simulans, D. sechellia and D. mauritiana: effects of population size and selection

Morton, R. A.; Choudhary, Madhu; Cariou, Marie‐Louise; Singh, Rama S.

doi:10.1007/978-94-007-0965-2_9

Cited by 11 publications

(7 citation statements)

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“…Even so, the collections of bottleneck times are in agreement with biogeographic evidences of the European expansion of this species, and hence the pattern of nucleotide variation observed at the OS region might reflect the founder effect caused by the recent colonization process. Although the range of putative bottleneck severities affecting the European population of D. simulans is similar to those estimates from derived populations of D. melanogaster Orengo and Aguade 2004;Thornton and Andolfatto 2006; but see Li and Stephan 2006), current bottleneck times are consistent with the hypothesis that D. simulans would have spread worldwide more recently than its sibling species (Morton et al 2004;Baudry et al 2006).…”

Section: Discussionsupporting

confidence: 75%

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

Sánchez-Gracia

Rozas

2007

Genetics

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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...

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Section: Discussionsupporting

confidence: 75%

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

Sánchez-Gracia

Rozas

2007

Genetics

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“…1; Table 1; Supplemental Table S3) and has been noted previously in the D. simulans-D. sechellia comparison (Singh et al 2008). Reduced divergence on the X chromosome compared with the autosomes could be explained by hybridization between species of the D. simulans clade (Ballard 2000;Morton et al 2004;Nunes et al 2010). If the X chromosome experiences more interspecific gene flow than the autosomes, this would result in a higher divergence on the autosomes.…”

Section: Resultsmentioning

confidence: 55%

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

Nolte¹,

Pandey²,

Kofler³

et al. 2012

Genome Res.

117

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Although it is well understood that selection shapes the polymorphism pattern in Drosophila, signatures of classic selective sweeps are scarce. Here, we focus on Drosophila mauritiana, an island endemic, which is closely related to Drosophila melanogaster. Based on a new, annotated genome sequence, we characterized the genome-wide polymorphism by sequencing pooled individuals (Pool-seq). We show that the interplay between selection and recombination results in a genome-wide polymorphism pattern characteristic for D. mauritiana. Two large genomic regions (>500 kb) showed the signature of almost complete selective sweeps. We propose that the absence of population structure and limited geographic distribution could explain why such pronounced sweep patterns are restricted to D. mauritiana. Further evidence for strong adaptive evolution was detected for several nucleoporin genes, some of which were not previously identified as genes involved in genomic conflict. Since this adaptive evolution is continuing after the split of D. mauritiana and Drosophila simulans, we conclude that genomic conflict is not restricted to short episodes, but rather an ongoing process in Drosophila.

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“…It is commonly thought that D. melanogaster expanded its range out of Africa in conjunction with the rise of agriculture after the Neolithic revolution $10,000 years ago (Lachaise et al 1988). On the basis of allozyme data, it has been suggested that D. simulans spread worldwide much more recently (Morton et al 2004).…”

Section: Discussionmentioning

confidence: 99%

Contrasted Polymorphism Patterns in a Large Sample of Populations From the Evolutionary Genetics Model Drosophila simulans

et al. 2006

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African populations of Drosophila simulans are thought to be ancestral in this model species and are increasingly used for testing general hypotheses in evolutionary genetics. It is often assumed that African populations are more likely to be at a neutral mutation drift equilibrium than other populations. Here we examine population structuring and the demographic profile in nine populations of D. simulans. We surveyed sequence variation in four X-linked genes (runt, sevenless, Sex-lethal, and vermilion) that have been used in a parallel study in the closely related species D. melanogaster. We found that an eastern group of populations from continental Africa and Indian Ocean islands (Kenya, Tanzania, Madagascar, and Mayotte Island) is widespread, shows little differentiation, and has probably undergone demographic expansion. The other two African populations surveyed (Cameroon and Zimbabwe) show no evidence of population expansion and are markedly differentiated from each other as well as from the populations from the eastern group. Two other populations, Europe and Antilles, are probably recent invaders to these areas. The Antilles population is probably derived from Europe through a substantial bottleneck. The history of these populations should be taken into account when drawing general conclusions from variation patterns. DROSOPHILA melanogaster and D. simulans are two cosmopolitan sibling species widely used in evolutionary studies. Despite their recent common ancestry, they show surprising differences in genomic parameters. Sequence variation parameters differ across chromosomes, across species, and between African and European populations. A number of hypotheses involving differences in history, in effective population size, in life history traits, and in chromosome inversion frequencies have been alleged for explaining these contrasts (see, e.g., Begun 1996; Moriyama and Powell 1996;Irvin et al. 1998;Andolfatto and Przeworski 2000;Andolfatto 2001;Charlesworth 2001;Capy and Gibert 2004;Gravot et al. 2004). A long and established history of studies has made these two species excellent models for evolutionary analyses. They have independently undergone a similar evolution and are thus considered useful systems for studying the critical factors involved in genetic evolution. Despite these strengths as model systems, population histories can add unique, contingent factors to the patterns of variation that can obscure patterns of change if they are not accounted for in data interpretation.Biometrical studies conducted in D. melanogaster by Teissier (1957) showed long ago that this species is geographically differentiated. More recent studies based on molecular markers have confirmed that African D. melanogaster populations are genetically differentiated (Bénassi and Veuille 1995;Michalakis and Veuille 1996;Veuille et al. 1998;Baudry et al. 2004). In D. simulans, Hamblin and Veuille (1999) studied two genes, vermilion (v) and Glucose-6 phosphate dehydrogenase (G6pd), in several populations from the Old ...

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A reanalysis of protein polymorphism in Drosophila melanogaster, D. simulans, D. sechellia and D. mauritiana: effects of population size and selection

Cited by 11 publications

References 4 publications

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

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

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

Contrasted Polymorphism Patterns in a Large Sample of Populations From the Evolutionary Genetics Model Drosophila simulans

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