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Genome-wide analysis of a long-term evolution experiment with Drosophila

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 yeast1,2,3. Here we present whole-genome resequencing data from Drosophila melanogaster populations that have experienced over 600 generations 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 polymorphisms, 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.

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Figure 1: Summary of phenotypic divergence in the selection treatments described in this study.
Figure 2: Differentiation throughout the genome.
Figure 3: Heterozygosity throughout the genome.
Figure 4: Analysis of individual genotypes, measured by cleaved amplified polymorphic sequence (CAPS) techniques.

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GenBank/EMBL/DDBJ

Data deposits

The FASTQ files associated with this project have been deposited in GenBank's Short Read Archive under the study accession number SRP002024. Data and source code files to reproduce the analyses of this work are available on request from the authors.

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Acknowledgements

We thank K. Aeling and D. Heck at the UCI DNA and Protein Microarray Facility for help with preparation and sequencing of the ACO1 library. The pooled ACO and CO libraries were sequenced at the University of Oregon High-Throughput Sequencing Facility, with advice from D. Turnbull. We are grateful to S. Nuzdhin, T. Turner and J. J. Emerson for providing suggestions during the conception of the project, and to O. Tenaillon and F. Barreto for comments on previous versions of the manuscript. We also thank A. K. Chippindale for discussion of the phenotype data. This work was supported by a UCI Faculty Research and Training Grant to M.R.R. and NSF DEB-0614429 to A.D.L. M.K.B. is supported by an NSF Graduate Fellowship in STEM K-12 Education (DGE-0638751).

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Authors

Contributions

M.K.B., P.S. and J.P.D. performed the laboratory experiments. M.K.B., K.R.T. and A.D.L. analysed the data. M.K.B., M.R.R. and A.D.L. designed the project, and M.K.B., K.R.T., M.R.R. and A.D.L. wrote the manuscript.

Corresponding authors

Correspondence to Molly K. Burke or Anthony D. Long.

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The authors declare no competing financial interests.

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Burke, M., Dunham, J., Shahrestani, P. et al. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587–590 (2010). https://doi.org/10.1038/nature09352

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