Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.
The sequencing of the 12 genomes of members of the genus Drosophila was taken as an opportunity to reevaluate the genetic and physical maps for 11 of the species, in part to aid in the mapping of assembled scaffolds. Here, we present an overview of the importance of cytogenetic maps to Drosophila biology and to the concepts of chromosomal evolution. Physical and genetic markers were used to anchor the genome assembly scaffolds to the polytene chromosomal maps for each species. In addition, a computational approach was used to anchor smaller scaffolds on the basis of the analysis of syntenic blocks. We present the chromosomal map data from each of the 11 sequenced non-Drosophila melanogaster species as a series of sections. Each section reviews the history of the polytene chromosome maps for each species, presents the new polytene chromosome maps, and anchors the genomic scaffolds to the cytological maps using genetic and physical markers. The mapping data agree with Muller's idea that the majority of Drosophila genes are syntenic. Despite the conservation of genes within homologous chromosome arms across species, the karyotypes of these species have changed through the fusion of chromosomal arms followed by subsequent rearrangement events. O NE of the primary strengths of the genus Drosophila as a model system has been the relative ease of generating detailed cytogenetic maps. Indeed, the first definitive mapping of genes to chromosomes Genetics 179: 1601-1655 ( July 2008) was performed in Drosophila melanogaster (Bridges 1916). The subsequent discovery of polytene chromosomes in the salivary glands in this same species (Painter 1934) and their codification into fine-structure genetic/ cytogenetic maps represents perhaps one of the first forays into ''genomics.'' Polytene maps (Bridges 1935;Lefevre 1976) provided an important genetic tool for mapping genes, for detecting genetic diversity within populations, and for inferring phylogenies among related species (Dobzhansky and Sturtevant 1938;Judd et al. 1972;Ashburner and Lemeunier 1976;Lemeunier and Ashburner 1976). Sturtevant and Tan (1937) laid the groundwork for comparative genomics when they established that genes within the chromosomal arms are conserved or syntenic among species. In an insightful melding of the gene mapping and evolutionary studies, H. J. Muller (1940) proposed that the genomes of Drosophila species were subdivided into a set of homologous elements represented by chromosome arms. What Muller (1940) noted, which was subsequently elaborated on by Sturtevant and Novitski (1941), was that the presumed homologs of identified mutant alleles within a chromosome arm of D. melanogaster were also confined to a single arm in other species within the genus where mapping data were available. Using D. melanogaster as a reference, Muller proposed that each of the five major chromosome arms plus the dot chromosome be given a letter designation (A-F) and that this nomenclature be used to identify equivalent linkage groups within the genus.The an...
The genetic basis of sexual isolation that contributes to speciation is one of the unsolved questions in evolutionary biology. Drosophila ananassae and Drosophila pallidosa are closely related, and postmating isolation has not developed between them. However, females of both species discriminate their mating partners, and this discrimination contributes to strong sexual isolation between them. By using surgical treatments, we demonstrate that male courtship songs play a dominant role in female mate discrimination. The absence of the song of D. pallidosa dramatically increased interspecies mating with D. ananassae females but reduced intraspecies mating with D. pallidosa females. Furthermore, genetic analysis and chromosomal introgression by repeated backcrosses to D. pallidosa males identified possible loci that control female discrimination in each species. These loci were mapped on distinct positions near the Delta locus on the middle of the left arm of the second chromosome. Because the mate discrimination we studied is well developed and is the only known mechanism that prevents gene flow between them, these loci may have played crucial roles in the evolution of reproductive isolation, and therefore, in the speciation process between these two species.
Drosophila ananassae and its relatives have many advantages as a model of genetic differentiation and speciation. In this report, we examine evolutionary relationships in the ananassae species subgroup using a multi-locus molecular data set, karyotypes, meiotic chromosome configuration, chromosomal inversions, morphological traits, and patterns of reproductive isolation. We describe several new taxa that are the closest known relatives of D. ananassae. Analysis of Y-chromosomal and mitochondrial haplotypes, shared chromosome arrangements, pre-mating isolation and hybrid male sterility suggests that these taxa represent a recent evolutionary radiation and may experience substantial gene flow. We discuss possible evolutionary histories of these species and give a formal description of one of them as D. parapallidosa Tobari sp. n. The comparative framework established by this study, combined with the recent sequencing of the D. ananassae genome, will facilitate future studies of reproductive isolation, phenotypic variation and genome evolution in this lineage.
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