%0 Journal Article %1 burke2010genomewide %A Burke, Molly K. %A Dunham, Joseph P. %A Shahrestani, Parvin %A Thornton, Kevin R. %A Rose, Michael R. %A Long, Anthony D. %D 2010 %I Nature Publishing Group %J Nature %K Drosophila experimental_evolution life_history scan_for_selection sequencing %N 7315 %P 587--590 %R 10.1038/nature09352 %T Genome-wide analysis of a long-term evolution experiment with Drosophila %U http://dx.doi.org/10.1038/nature09352 %V 467 %X Experimental evolution systems allow the genomic study of adaptation, and so far this has been done primarily in asexual systems with small genomes, such as bacteria and yeast 1–3 . Here we present whole-genome resequencing data from Drosophila melanogaster populations that have experienced over 600 genera- tions of laboratory selection for accelerated development. Flies in these selected populations develop from egg to adult ,20% faster than flies of ancestral control populations, and have evolved a number of other correlated phenotypes. On the basis of 688,520 intermediate-frequency, high-quality single nucleotide poly- morphisms, we identify several dozen genomic regions that show strong allele frequency differentiation between a pooled sample of five replicate populations selected for accelerated development and pooled controls. On the basis of resequencing data from a single replicate population with accelerated development, as well as single nucleotide polymorphism data from individual flies from each replicate population, we infer little allele frequency differentiation between replicate populations within a selection treatment. Signatures of selection are qualitatively different than what has been observed in asexual species; in our sexual populations, adaptation is not associated with ‘classic’ sweeps whereby newly arising, unconditionally advantageous mutations become fixed. More parsimonious explanations include ‘incomplete’ sweep models, in which mutations have not had enough time to fix, and ‘soft’ sweep models, in which selection acts on pre-existing, common genetic variants. We conclude that, at least for life history characters such as development time, unconditionally advantageous alleles rarely arise, are associated with small net fitness gains or cannot fix because selection coefficients change over time. Experimental evolution uses well-defined selection protocols to force phenotypic divergence 4,5 . Studies of experimentally evolved popula- tions have identified mutations responsible for particular adaptations 6 and provided some general insights into the nature of adaptation in asexually reproducing populations 7 . Adaptation in these populations is driven by so-called classic selective sweeps, or the fixation of newly arising beneficial mutations and the genome-wide haplotypes asso- ciated with them. By contrast, an obligate sexually reproducing system can harbour a great deal of standing genetic variation on which selection can act. Standing variation is theoretically predicted to lead to rapid evolution in novel environments 8 , and case studies of ecologically rel- evant genes bear out this prediction 9–11 . The idea that short-term evolu- tion may act primarily on pre-existing intermediate-frequency genetic variants that are swept the remainder of the way to fixation has been termed a soft sweep 8,12 model. We collected genome-wide resequence data for outbred, sexually reproducing, replicated populations of D. melanogaster selected for accelerated development and their matched control populations. Using the Illumina platform, we obtained short-read sequences from three genomic DNA libraries: a pooled sample of five replicate popula- tions that have undergone sustained selection for accelerated develop- ment and early fertility for over 600 generations (ACO); a pooled sample of five replicate ancestral control populations, which experi- ence no direct selection on development time (CO); and a single ACO replicate population (ACO 1 ). The ACO treatment has evolved strongly differentiated life history phenotypes relative to those of the CO treat- ment 13 (summarized in Fig. 1; see also Supplementary Fig. 1 for the history of the populations). To identify single nucleotide polymorphisms (SNPs) significantly differentiated between the ACO and CO populations, we aligned reads to the reference genome of Drosophila and considered only those genomic positions at which there were two observed allelic states. After quality-filtering, we were left with 688,520 SNPs: approximately one SNP for every 175 base pairs (bp) on the 120-megabase (Mb) euchromatic genome (Methods). The average alignment depth at identified SNPs was ,203 in both the ACO and CO libraries (Supplementary Fig. 2), and ,103 in the ACO 1 library. For every SNP, we calculated 2log 10 (P) from a Fisher’s exact test (L 10 FET) for a difference in allele frequency between the ACO and CO libraries, as well as the ACO and ACO 1 libraries.

@article{burke2010genomewide, abstract = {Experimental evolution systems allow the genomic study of adaptation, and so far this has been done primarily in asexual systems with small genomes, such as bacteria and yeast 1–3 . Here we present whole-genome resequencing data from Drosophila melanogaster populations that have experienced over 600 genera- tions of laboratory selection for accelerated development. Flies in these selected populations develop from egg to adult ,20% faster than flies of ancestral control populations, and have evolved a number of other correlated phenotypes. On the basis of 688,520 intermediate-frequency, high-quality single nucleotide poly- morphisms, we identify several dozen genomic regions that show strong allele frequency differentiation between a pooled sample of five replicate populations selected for accelerated development and pooled controls. On the basis of resequencing data from a single replicate population with accelerated development, as well as single nucleotide polymorphism data from individual flies from each replicate population, we infer little allele frequency differentiation between replicate populations within a selection treatment. Signatures of selection are qualitatively different than what has been observed in asexual species; in our sexual populations, adaptation is not associated with ‘classic’ sweeps whereby newly arising, unconditionally advantageous mutations become fixed. More parsimonious explanations include ‘incomplete’ sweep models, in which mutations have not had enough time to fix, and ‘soft’ sweep models, in which selection acts on pre-existing, common genetic variants. We conclude that, at least for life history characters such as development time, unconditionally advantageous alleles rarely arise, are associated with small net fitness gains or cannot fix because selection coefficients change over time. Experimental evolution uses well-defined selection protocols to force phenotypic divergence 4,5 . Studies of experimentally evolved popula- tions have identified mutations responsible for particular adaptations 6 and provided some general insights into the nature of adaptation in asexually reproducing populations 7 . Adaptation in these populations is driven by so-called classic selective sweeps, or the fixation of newly arising beneficial mutations and the genome-wide haplotypes asso- ciated with them. By contrast, an obligate sexually reproducing system can harbour a great deal of standing genetic variation on which selection can act. Standing variation is theoretically predicted to lead to rapid evolution in novel environments 8 , and case studies of ecologically rel- evant genes bear out this prediction 9–11 . The idea that short-term evolu- tion may act primarily on pre-existing intermediate-frequency genetic variants that are swept the remainder of the way to fixation has been termed a soft sweep 8,12 model. We collected genome-wide resequence data for outbred, sexually reproducing, replicated populations of D. melanogaster selected for accelerated development and their matched control populations. Using the Illumina platform, we obtained short-read sequences from three genomic DNA libraries: a pooled sample of five replicate popula- tions that have undergone sustained selection for accelerated develop- ment and early fertility for over 600 generations (ACO); a pooled sample of five replicate ancestral control populations, which experi- ence no direct selection on development time (CO); and a single ACO replicate population (ACO 1 ). The ACO treatment has evolved strongly differentiated life history phenotypes relative to those of the CO treat- ment 13 (summarized in Fig. 1; see also Supplementary Fig. 1 for the history of the populations). To identify single nucleotide polymorphisms (SNPs) significantly differentiated between the ACO and CO populations, we aligned reads to the reference genome of Drosophila and considered only those genomic positions at which there were two observed allelic states. After quality-filtering, we were left with 688,520 SNPs: approximately one SNP for every 175 base pairs (bp) on the 120-megabase (Mb) euchromatic genome (Methods). The average alignment depth at identified SNPs was ,203 in both the ACO and CO libraries (Supplementary Fig. 2), and ,103 in the ACO 1 library. For every SNP, we calculated 2log 10 (P) from a Fisher’s exact test (L 10 FET) for a difference in allele frequency between the ACO and CO libraries, as well as the ACO and ACO 1 libraries.}, added-at = {2016-04-01T22:23:10.000+0200}, author = {Burke, Molly K. and Dunham, Joseph P. and Shahrestani, Parvin and Thornton, Kevin R. and Rose, Michael R. and Long, Anthony D.}, biburl = {https://www.bibsonomy.org/bibtex/2af653aef7af5a0c56ac9eb68075d7db4/peter.ralph}, doi = {10.1038/nature09352}, interhash = {c1f39c97e767b375f22a3d344c538e73}, intrahash = {af653aef7af5a0c56ac9eb68075d7db4}, issn = {00280836}, journal = {Nature}, keywords = {Drosophila experimental_evolution life_history scan_for_selection sequencing}, month = sep, number = 7315, pages = {587--590}, publisher = {Nature Publishing Group}, timestamp = {2016-04-01T22:23:10.000+0200}, title = {Genome-wide analysis of a long-term evolution experiment with {Drosophila}}, url = {http://dx.doi.org/10.1038/nature09352}, volume = 467, year = 2010 }