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...
North America and South America have recently been colonized by the Palearctic species Drosophila subobscura. This double colonization offers a rare opportunity for evolutionary studies. Correlations between chromosomal arrangement frequencies and latitude were calculated for the colonizing populations. Signs of these correlations are highly coincident with those found in the Old World. These results provide experimental support for the adaptive value of the chromosomal-inversion polymorphism; historical and other nonadaptive explanations are thus excluded or relegated to a secondary role.
Synonymous codons are not generally used at equal frequencies, and this trend is observed for most genes and organisms. Several methods have been proposed and used to estimate the degree of the nonrandom use of the different synonymous codons. The estimates obtained by these methods, however, show different levels of both precision and dispersion when coding regions of a finite number of codons are under analysis. Here, we present a study, based on computer simulation, of how the different methods proposed to evaluate the nonrandom use of synonymous codons are affected by the length of the coding region analyzed. The results show that some of these methods are heavily influenced by the number of codons and that the comparison of codon usage bias between coding regions of different lengths shows a methodological bias under different conditions of nonrandom use of synonymous codons. The study of the dispersion of the estimates obtained by the different methods gives, on the other hand, an indication of the methods to be applied to compare values of codon usage bias among coding regions of equivalent length.
The neutral theory of molecular evolution predicts that regions of the genome that evolve at high rates, as revealed by interspecific DNA sequence comparisons, will also exhibit high levels of polymorphism within species. We present here a conservative statistical test of this prediction based on a constant-rate neutral model. The test requires data from an interspecific comparison of at least two regions of the genome and data on levels of intraspecific polymorphism in the same regions from at least one species. The model is rejected for data from the region encompassing the Adh locus and the 5′ flanking sequence of Drosophila melanogaster and Drosophila sechellia. The data depart from the model in a direction that is consistent with the presence of balanced polymorphism in the coding region.
Nucleotide variation in eight effectively unlinked genes was surveyed in species-wide samples of the closely related outbreeding species Arabidopsis halleri and A. lyrata ssp. petraea and in three of these genes in A. lyrata ssp. lyrata and A. thaliana. Significant genetic differentiation was observed more frequently in A. l. petraea than in A. halleri. Average estimates of nucleotide variation were highest in A. l. petraea and lowest in A. l. lyrata, reflecting differences among species in effective population size. The low level of variation in A. l. lyrata is concordant with a bottleneck effect associated with its origin. The A. halleri/A. l. petraea speciation process was studied, considering the orthologous sequences of an outgroup species (A. thaliana). The high number of ancestral mutations relative to exclusive polymorphisms detected in A. halleri and A. l. petraea, the significant results of the multilocus Fay and Wu H tests, and haplotype sharing between the species indicate introgression subsequent to speciation. Average among-population variation in A. halleri and A. l. petraea was -5.1ف and 3-fold higher than that in the inbreeder A. thaliana. The detected reduction of variation in A. thaliana is less than that expected from differences in mating system alone, and therefore from selective processes related to differences in the effective recombination rate, but could be explained by differences in population structure.
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