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.

We have sequenced the genome of a second Drosophila species, Drosophila pseudoobscura, and compared this to the genome sequence of Drosophila melanogaster, a primary model organism. Throughout evolution the vast majority of Drosophila genes have remained on the same chromosome arm, but within each arm gene order has been extensively reshuffled, leading to a minimum of 921 syntenic blocks shared between the species. A repetitive sequence is found in the D. pseudoobscura genome at many junctions between adjacent syntenic blocks. Analysis of this novel repetitive element family suggests that recombination between offset elements may have given rise to many paracentric inversions, thereby contributing to the shuffling of gene order in the D. pseudoobscura lineage. Based on sequence similarity and synteny, 10,516 putative orthologs have been identified as a core gene set conserved over 25-55 million years (Myr) since the pseudoobscura/melanogaster divergence. Genes expressed in the testes had higher amino acid sequence divergence than the genome-wide average, consistent with the rapid evolution of sex-specific proteins. Cis-regulatory sequences are more conserved than random and nearby sequences between the species-but the difference is slight, suggesting that the evolution of cis-regulatory elements is flexible. Overall, a pattern of repeat-mediated chromosomal rearrangement, and high coadaptation of both male genes and cis-regulatory sequences emerges as important themes of genome divergence between these species of Drosophila.

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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 population genetic consequences of nearestneighbor pollination in an outcrossing plant species were investigated through computer simulations. The genetic system consisted of two alleles at a single locus in a self-incompatible plant that mates by random pollen transfer from a neighboring individual. Beginning with a random distribution ofgenotypes, restricted pollen and seed dispersal were applied each generation to 10,000 individuals spaced uniformly on a square grid. This restricted gene flow caused inbreeding, a rapid increase in homozygosity, and striking microgeographic differentiation of the populations. Patches of homozygotes bordered by heterozygotes formed quickly and persisted for many generations. Thus, high levels of inbreeding, homozygosity, and patchiness in the spatial distribution of genotypes are expected in plant populations with breeding systems based on nearest-neighbor pollination, and such observations require no explanation by natural selection or other deterministic forces.Genetic differentiation of populations over the habitats they occupy is a major factor in the processes of adaptation and evolution. For populations subdivided into small colonies, it is easy to picture this differentiation as the result of genetic drift. Wright (1-3) showed that even large populations distributed continuously over an area will differentiate if gene dispersal within them is sufficiently restricted. He termed this process isolation by distance. Many genetic characteristics of such continuous populations depend on the size of local breeding units, or neighborhoods, within them. In particular, the smaller the neighborhoods, the greater the genetic differentiation in the population, so these neighborhoods are essentially subdivisions created by limited gene dispersal. Inbreeding and increased homozygosity result, as does a spatial differentiation ofgene and genotype frequencies. The genetic structure of a population departs considerably from that expected in a random-mating population. Rohlf and Schnell (4), using computer simulations of Wright's model to examine spatial patterning and genetic differentiation in populations with various neighborhood sizes, observed rapid establishment of spatial patterns in gene frequency, which persisted for many generations.Many plant species have reproductive systems ideally suited to isolation by distance. Pollinator flight behavior and seed dispersal determine gene flow, and both are often severely limited. The restriction on pollen movement is particularly strong when pollinators fly between nearest-neighboring plants, a common behavior. Levin and Kerster (5), for example, observed almost exclusively nearest-neighbor pollination (NNP) in Liatris aspera (Compositae), as well as highly localized dispersal of seeds. Even with some carryover ofpollen from previous visits, gene dispersal was highly leptokurtic (6). NNP has been reported sufficiently often for other plants and pollinators (5-15) that it is clearly an important characteristic of pollination bio...

Drosophila pseudoobscura harbors a rich polymorphism for paracentric inversions on the third chromosome, and the clines in the inversion frequencies across the southwestern United States indicate that strong natural selection operates on them. Isogenic inversion strains were made from isofemale lines collected from four localities, and eight molecular markers were mapped on the third chromosome. Nucleotide diversity was measured for these loci and formed the basis of an evolutionary genomic analysis. The loci were differentiated among inversions. The inversions did not show significant differences among populations, however, likely the result of extensive gene flow among populations. Some loci had significant reductions in nucleotide diversity within inversions compared with interspecies divergence, suggesting that these loci are near inversion breakpoints or are near targets of directional selection. Linkage disequilibrium (LD) levels tended to decrease with distance between loci, indicating that some genetic exchange occurs among gene arrangements despite the presence of inversions. In some cases, however, adjacent genes had low levels of interlocus LD and loosely linked genes had high levels of interlocus LD, suggesting strong epistatic selection. Our results support the hypothesis that the inversions of D. pseudoobscura have emerged as suppressors of recombination to maintain positive epistatic relationships among loci within gene arrangements that developed as the species adapted to a heterogeneous environment.

The Compensation Hypothesis says that parents and prospective parents attempt to make up for lowered offspring viability by increasing reproductive effort to produce healthy, competitive offspring and by increasing investment in less viable, but still-living progeny (parental effects). The hypothesis assumes that offspring viability is lower when individuals are constrained (often through sexual conflict) to breed with individuals they do not prefer. We review results of experimental tests of the offspring-viability assumption in Tanzanian cockroaches, fruit flies, pipefish, wild mallards, and feral house mice. Experimental constraints on mating preferences lowered offspring viability in each of the studies. Females breeding under constraints laid more eggs or gave birth to more young than females breeding without or with fewer constraints on their mating preferences, and males mating under constraints on their mate preferences ejaculated more sperm than males mating without constraints. The number of eggs laid or offspring born was higher when female choosers were experimentally constrained to reproduce with males they did not prefer. Constrained females may increase fecundity to enhance the probability that they produce adult offspring with rarer phenotypes with survival benefits against offspring generation pathogens. Similarly, ejaculation of more sperm when males are paired with females they do not prefer may be a mechanism that provides more variable sperm haplotypes for prospective mothers or that may provide nutritional benefits to mothers and zygotes. differential allocation ͉ fecundity ͉ sexual conflict ͉ constraints hypothesis T he Compensation Hypothesis (CH) (1, 2) says that parents and prospective parents increase reproductive effort and investments in offspring to make up for lowered offspring viability resulting from reproduction under constraints. It predicts what individuals do when they are unable to mate with preferred partners as often happens under sexual conflict, i.e., when individuals are constrained to reproduce with partners they do not prefer. The hypothesis assumes that (i) when constrained individuals have other options, they resist reproduction with partners they do not prefer, but sometimes resistance is unsuccessful and individuals then attempt to make the best of a bad job; and (ii) constraints on the free expression of mate preferences negatively affect offspring viability. In this work, we introduce the assumptions and predictions of the CH; in Results and Discussion we describe combined analyses over independent studies designed to test the assumptions and predictions of the CH, and we contrast our results with predictions from classical sexual selection.

Using a computer simulation, we have examined the dynamics of recombinational speciation, a potentially rapid mode of evolution dependent on chromosomal reassortment in populations of partially sterile interspecific hybrids. We describe how various parameters affect the time required for a new recombinant species to become established within the setting of a spatially structured hybrid zone. Our results indicate that recombinational speciation is most likely to occur where (1) the hybrid zone interface is long, (2) the organisms involved are predominantly selfing, (3) the hybrids are relatively fertile, and (4) the number of differences in chromosomal structure between the parental species is small. The speciation dynamics are characterized by long-term stasis followed by an abrupt transition to a new reproductively isolated type. The results are largely the same whether the nascent recombinant species is favoured by a fertility or a viability advantage. Recombinational speciation, like polyploidy, appears to be a feasible mechanism for sympatric speciation in plants.