Genome-wide analysis of a long-term evolution experiment with Drosophila (original) (raw)
- Letter
- Published: 15 September 2010
- Joseph P. Dunham2,3,
- Parvin Shahrestani1,
- Kevin R. Thornton1,
- Michael R. Rose1 &
- …
- Anthony D. Long1
Nature volume 467, pages 587–590 (2010)Cite this article
- 9757 Accesses
- 318 Citations
- 53 Altmetric
- Metrics details
Subjects
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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Additional access options:
Similar content being viewed by others
Accession codes
Primary accessions
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.
References
- Papadopoulos, D. et al. Genomic evolution during a 10,000-generation experiment with bacteria. Proc. Natl Acad. Sci. USA 96, 3807–3812 (1999)
Article ADS CAS PubMed PubMed Central Google Scholar - Dunham, M. J. et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae . Proc. Natl Acad. Sci. USA 99, 16144–16149 (2002)
Article ADS CAS PubMed PubMed Central Google Scholar - Hegreness, M. & Kishony, R. Analysis of genetic systems using experimental evolution and whole-genome sequencing. Genome Biol. 8, 201 (2007)
Article PubMed PubMed Central Google Scholar - Garland, T. & Rose, M. R. Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments (Univ. California Press, 2009)
Google Scholar - Teotónio, H., Chelo, I. M., Bradic, M., Rose, M. R. & Long, A. D. Experimental evolution reveals natural selection on standing genetic variation. Nature Genet. 41, 251–257 (2009)
Article PubMed Google Scholar - Herring, C. D. et al. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nature Genet. 38, 1406–1412 (2006)
Article CAS PubMed Google Scholar - Barrick, J. E. et al. Genome evolution and adaptation in a long-term experiment with Escherichia coli . Nature 461, 1243–1247 (2009)
Article ADS CAS PubMed Google Scholar - Hermisson, J. & Pennings, P. S. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335–2352 (2005)
Article CAS PubMed PubMed Central Google Scholar - Feder, J. L. et al. Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proc. Natl Acad. Sci. USA 100, 10314–10319 (2003)
Article ADS CAS PubMed PubMed Central Google Scholar - Pelz, H. J. et al. The genetic basis of resistance to anticoagulants in rodents. Genetics 170, 1839–1847 (2005)
Article CAS PubMed PubMed Central Google Scholar - Colosimo, P. F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307, 1928–1933 (2005)
Article ADS CAS PubMed Google Scholar - Przeworski, M., Coop, G. & Wall, J. D. The signature of positive selection on standing genetic variation. Evolution 59, 2312–2323 (2005)
Article PubMed Google Scholar - Rose, M. R., Passananti, H. B. & Matos, M. Methuselah Flies: A Case Study in the Evolution of Aging (World Scientific, 2004)
Book Google Scholar - Hoekstra, H. E. & Coyne, J. A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995–1016 (2007)
Article PubMed Google Scholar - Dennis, G. et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4, R60 (2003)
Article PubMed Central Google Scholar - Kaplan, N. L., Hudson, R. R. & Langley, C. H. The hitchhiking effect revisited. Genetics 123, 887–899 (1989)
CAS PubMed PubMed Central Google Scholar - Innan, H. & Kim, Y. Pattern of polymorphism after strong artificial selection in a domestication event. Proc. Natl Acad. Sci. USA 101, 10667–10672 (2004)
Article ADS CAS PubMed PubMed Central Google Scholar - Teotónio, H. & Rose, M. R. Variation in the reversibility of evolution. Nature 408, 463–466 (2000)
Article ADS PubMed Google Scholar - Chevin, L. M. & Hospital, F. Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 180, 1645–1660 (2008)
Article PubMed PubMed Central Google Scholar - Chippindale, A. K., Alipaz, J. A., Chen, H. W. & Rose, M. R. Experimental evolution of accelerated development in Drosophila. 1. Developmental speed and larval survival. Evolution 51, 1536–1551 (1997)
Article PubMed Google Scholar - Chippindale, A. K., Alipaz, J. A. & Rose, M. R. in Methuselah Flies (eds Rose, M. R., Passananti, H. B. & Matos, M.) 413–435 (World Scientific, 2004)
Book Google Scholar - Bloom, J. S., Khan, Z., Kruglyak, L., Singh, M. & Caudy, A. A. Measuring differential gene expression by short read sequencing: quantitative comparison to 2-channel gene expression microarrays. BMC Genomics 10, 221 (2009)
Article PubMed PubMed Central Google Scholar
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).
Author information
Authors and Affiliations
- Ecology and Evolutionary Biology, University of California, Irvine, 321 Steinhaus Hall, Irvine, California 92697-2525, USA ,
Molly K. Burke, Parvin Shahrestani, Kevin R. Thornton, Michael R. Rose & Anthony D. Long - Molecular and Computational Biology, University of Southern California,
Joseph P. Dunham - Los Angeles, 90098, California, USA
Joseph P. Dunham
Authors
- Molly K. Burke
You can also search for this author inPubMed Google Scholar - Joseph P. Dunham
You can also search for this author inPubMed Google Scholar - Parvin Shahrestani
You can also search for this author inPubMed Google Scholar - Kevin R. Thornton
You can also search for this author inPubMed Google Scholar - Michael R. Rose
You can also search for this author inPubMed Google Scholar - Anthony D. Long
You can also search for this author inPubMed Google Scholar
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 toMolly K. Burke or Anthony D. Long.
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-7 with legends and Supplementary Tables 1-2. (PDF 1877 kb)
PowerPoint slides
Rights and permissions
About this article
Cite this article
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
- Received: 05 April 2010
- Accepted: 15 July 2010
- Published: 15 September 2010
- Issue Date: 30 September 2010
- DOI: https://doi.org/10.1038/nature09352
This article is cited by
Editorial Summary
Experimental evolution reveals resistance to change
Until now, experimental evolution has been largely performed in asexual systems with small genomes, such as bacteria and yeast. Burke et al. report results of a genome-wide study in Drosophila melanogaster fruitfly populations, which were selected in the lab for more than 600 generations to develop rapidly from egg to adult. In contrast to what is seen in asexual populations, the authors report 'soft' selective sweeps in which selection acts on pre-existing, common genetic variants, and conclude that unconditionally advantageous alleles rarely arise, are associated with small net fitness gains, or cannot fix because selection coefficients change over time.