Genomic Variation in Natural Populations ofDrosophila melanogaster

Abstract

This report of independent genome sequences of two natural populations of Drosophila melanogaster (37 from North America and 6 from Africa) provides unique insight into forces shaping genomic polymorphism and divergence. Evidence of interactions between natural selection and genetic linkage is abundant not only in centromere-and telomere-proximal regions, but also throughout the euchromatic arms. Linkage disequilibrium, which decays within 1 kbp, exhibits a strong bias toward coupling of the more frequent alleles and provides a high-resolution map of recombination rate. The juxtaposition of population genetics statistics in small genomic windows with gene structures and chromatin states yields a rich, high-resolution annotation, including the following: (1) 59-and 39-UTRs are enriched for regions of reduced polymorphism relative to lineage-specific divergence; (2) exons overlap with windows of excess relative polymorphism; (3) epigenetic marks associated with active transcription initiation sites overlap with regions of reduced relative polymorphism and relatively reduced estimates of the rate of recombination; (4) the rate of adaptive nonsynonymous fixation increases with the rate of crossing over per base pair; and (5) both duplications and deletions are enriched near origins of replication and their density correlates negatively with the rate of crossing over. Available demographic models of X and autosome descent cannot account for the increased divergence on the X and loss of diversity associated with the out-of-Africa migration. Comparison of the variation among these genomes to variation among genomes from D. simulans suggests that many targets of directional selection are shared between these species. A CCESS to sequenced genomes from natural, outbreeding populations (Begun et al. 2007; Li and Durbin 2011) places our theoretical understanding of the forces that determine patterns of genomic variation within and between taxa in a new empirical light. Alignment of the predictions of classical evolutionary genetic models with richly annotated population genomic survey data is an exciting challenge. Descriptions of the patterns of variation in these first sets of population genomic data can foster efficient sieving of hypotheses and serve as a foundation for the design of subsequent studies. Here we present the description of the genomic sequence assemblies from two collections of natural populations of Drosophila melanogaster. The polymorphism, divergence, and copy-number variation revealed in these data are presented at several scales that all support the hypothesis by Maynard Smith and Haigh (1974) The study of genetic variation in natural populations of D. melanogaster has played an important role in the development of evolutionary theory, largely because of the central role of the species in the advancement of knowledge of genetic inheritance. Our fundamental understanding of the biology of D. melanogaster, as well as the advanced methods and unique resources available for its study, has fuel...

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

“…Nucleoporin genes, implicated in hybrid incompatibilities that have evolved between D. simulans and D. melanogaster, are possible targets of recurrent positive selection due to ongoing genomic conflict (Presgraves and Stephan 2007). Unlike previous genome-wide polymorphism surveys of D. simulans and D. melanogaster Langley et al 2012), we find that in the D. mauritiana lineage, nucleoporins are among the genes showing the strongest evidence of recurrent adaptive evolution. Furthermore, the presence of a pair of meiotic drive genes and a ''speciation'' gene at the center of two valleys of strongly reduced variability suggests that these sweeps have been caused by genes involved in genomic conflict.…”

Effects of Linked Selective Sweeps on Demographic Inference and Model Selection

“…This is a very small number indeed, equivalent to a single recent sweep affecting ,1% of all genes. Indeed in Drosophila the fraction of loci affected by recent positive selection may be quite large (Begun et al 2007;Langley et al 2012). Numerous studies have estimated that the fraction of adaptive amino acid substitutions in D. melanogaster is considerable, with estimates ranging from 10 to 50% (Smith and EyreWalker 2002;Bierne and Eyre-Walker 2004;Langley et al 2012;Mackay et al 2012).…”

“…Indeed in Drosophila the fraction of loci affected by recent positive selection may be quite large (Begun et al 2007;Langley et al 2012). Numerous studies have estimated that the fraction of adaptive amino acid substitutions in D. melanogaster is considerable, with estimates ranging from 10 to 50% (Smith and EyreWalker 2002;Bierne and Eyre-Walker 2004;Langley et al 2012;Mackay et al 2012). Direct estimates of the rate of recurrent hitchhiking in Drosophila populations also indicate a substantial flux of adaptive substitution, with the population effective sweep rate varying between 1.1 3 10 25 and 2.6 3 10 23 sweeps per base pair per 2N generations (Li and Stephan 2006;Andolfatto 2007;Macpherson et al 2007;Jensen et al 2008).…”

High nucleotide diversity and limited linkage disequilibrium in Helicoverpa armigera facilitates the detection of a selective sweep

“…In Aedes aegypti, Anopheles funestus and Anopheles gambiae for instance, nucleotide diversity in noncoding regions is approximately 0.01; in Drosophila melanogaster it is~0.01 and in D. simulans it is~0.02 (Morlais and Severson, 2003;Wondji et al, 2007;Langley et al, 2012;O'Loughlin et al, 2014). It is worth noting that, if the mutation rates differ between the sexes, then nucleotide diversity at neutral loci can differ between sex chromosomes and autosomes (Vicoso and Charlesworth, 2006).…”