This Article Full Text Full Text (PDF) Supplemental Research Data Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Haddrill, P. R. Articles by Andolfatto, P. Search for Related Content PubMed PubMed Citation Articles by Haddrill, P. R. Articles by Andolfatto, P. Pubmed/NCBI databases Nucleotide Social Bookmarking                   What's this?

Letter

Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations

¹ Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, EH9 3JT, United Kingdom ² Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853, USA ³ Section of Ecology, Behavior and Evolution, Division of Biological Sciences, University of California San Diego, La Jolla, California 92093, USA

Uncertainty about the demographic history of populations can hamper genome-wide scans for selection based on population genetic models. To obtain a portrait of the effects of demographic history on genome variability patterns in Drosophila melanogaster populations, we surveyed noncoding DNA polymorphism at 10 X-linked loci in large samples from three African and two non-African populations. All five populations show significant departures from expectations under the standard neutral model. We detect weak but significant differentiation between East (Kenya and Zimbabwe) and West/Central sub-Saharan (Gabon) African populations. A skew toward high-frequency-derived polymorphisms, elevated levels of linkage disequilibrium (LD) and significant heterogeneity in levels of polymorphism and divergence in the Gabon sample suggest that this population is further from mutation-drift equilibrium than the two Eastern African populations. Both non-African populations harbor significantly higher levels of LD, a large excess of high-frequency-derived mutations and extreme heterogeneity among loci in levels of polymorphism and divergence. Rejections of the neutral model in D. melanogaster populations using these and similar features have been interpreted as evidence for an important role for natural selection in shaping genome variability patterns. Based on simulations, we conclude that simple bottleneck models are sufficient to account for most, if not all, polymorphism features of both African and non-African populations. In contrast, we show that a steady-state recurrent hitchhiking model fails to account for several aspects of the data. Demographic departures from equilibrium expectations in both ancestral and derived populations thus represent a serious challenge to detecting positive selection in genome-wide scans using current methodologies.

[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank under accession nos. AY925214-AY926258. The following individuals kindly provided reagents, samples, or unpublished information as indicated in the paper: B. Ballard, A. Clark, and A. Davis.]

Article and publication are at http://www.genome.org/cgi/doi/10.1101/gr.3541005.

CiteULike    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

				J. E. Pool and R. Nielsen The Impact of Founder Events on Chromosomal Variability in Multiply Mating Species Mol. Biol. Evol., August 1, 2008; 25(8): 1728 - 1736. [Abstract] [Full Text] [PDF]

				J. J. Emerson, M. Cardoso-Moreira, J. O. Borevitz, and M. Long Natural Selection Shapes Genome-Wide Patterns of Copy-Number Polymorphism in Drosophila melanogaster Science, June 20, 2008; 320(5883): 1629 - 1631. [Abstract] [Full Text] [PDF]

				A. Kawabe, A. Forrest, S. I. Wright, and D. Charlesworth High DNA Sequence Diversity in Pericentromeric Genes of the Plant Arabidopsis lyrata Genetics, June 1, 2008; 179(2): 985 - 995. [Abstract] [Full Text] [PDF]

				A. Ramirez-Soriano, S. E. Ramos-Onsins, J. Rozas, F. Calafell, and A. Navarro Statistical Power Analysis of Neutrality Tests Under Demographic Expansions, Contractions and Bottlenecks With Recombination Genetics, May 1, 2008; 179(1): 555 - 567. [Abstract] [Full Text] [PDF]

				I. J. Tsai, D. Bensasson, A. Burt, and V. Koufopanou Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle PNAS, March 25, 2008; 105(12): 4957 - 4962. [Abstract] [Full Text] [PDF]

				H. Chen, P. L. Morrell, M. de la Cruz, and M. T. Clegg Nucleotide Diversity and Linkage Disequilibrium in Wild Avocado (Persea americana Mill.) J. Hered., March 14, 2008; (2008) esn016v1. [Abstract] [Full Text] [PDF]

				E. Eveno, C. Collada, M. A. Guevara, V. Leger, A. Soto, L. Diaz, P. Leger, S. C. Gonzalez-Martinez, M. T. Cervera, C. Plomion, et al. "Contrasting Patterns of Selection at Pinus pinaster Ait. Drought Stress Candidate Genes as Revealed by Genetic Differentiation Analyses" Mol. Biol. Evol., February 1, 2008; 25(2): 417 - 437. [Abstract] [Full Text] [PDF]

				V. Nolte and C. Schlotterer African Drosophila melanogaster and D. simulans Populations Have Similar Levels of Sequence Variability, Suggesting Comparable Effective Population Sizes Genetics, January 1, 2008; 178(1): 405 - 412. [Abstract] [Full Text] [PDF]

				J. M. Macpherson, G. Sella, J. C. Davis, and D. A. Petrov Genomewide Spatial Correspondence Between Nonsynonymous Divergence and Neutral Polymorphism Reveals Extensive Adaptation in Drosophila Genetics, December 1, 2007; 177(4): 2083 - 2099. [Abstract] [Full Text] [PDF]

				S. De Mita, J. Ronfort, H. I. McKhann, C. Poncet, R. El Malki, and T. Bataillon Investigation of the Demographic and Selective Forces Shaping the Nucleotide Diversity of Genes Involved in Nod Factor Signaling in Medicago truncatula Genetics, December 1, 2007; 177(4): 2123 - 2133. [Abstract] [Full Text] [PDF]

				T. Pyhajarvi, M. R. Garcia-Gil, T. Knurr, M. Mikkonen, W. Wachowiak, and O. Savolainen Demographic History Has Influenced Nucleotide Diversity in European Pinus sylvestris Populations Genetics, November 1, 2007; 177(3): 1713 - 1724. [Abstract] [Full Text] [PDF]

				J. D. Jensen, V. L. Bauer DuMont, A. B. Ashmore, A. Gutierrez, and C. F. Aquadro Patterns of Sequence Variability and Divergence at the diminutive Gene Region of Drosophila melanogaster: Complex Patterns Suggest an Ancestral Selective Sweep Genetics, October 1, 2007; 177(2): 1071 - 1085. [Abstract] [Full Text] [PDF]

				S. Hutter, H. Li, S. Beisswanger, D. De Lorenzo, and W. Stephan Distinctly Different Sex Ratios in African and European Populations of Drosophila melanogaster Inferred From Chromosomewide Single Nucleotide Polymorphism Data Genetics, September 1, 2007; 177(1): 469 - 480. [Abstract] [Full Text] [PDF]

				D. A. Moeller, M. I. Tenaillon, and P. Tiffin Population Structure and Its Effects on Patterns of Nucleotide Polymorphism in Teosinte (Zea mays ssp. parviglumis) Genetics, July 1, 2007; 176(3): 1799 - 1809. [Abstract] [Full Text] [PDF]

				D. J. Orengo and M. Aguade Genome Scans of Variation and Adaptive Change: Extended Analysis of a Candidate Locus Close to the phantom Gene Region in Drosophila melanogaster Mol. Biol. Evol., May 1, 2007; 24(5): 1122 - 1129. [Abstract] [Full Text] [PDF]

				J. F. Baines and B. Harr Reduced X-Linked Diversity in Derived Populations of House Mice Genetics, April 1, 2007; 175(4): 1911 - 1921. [Abstract] [Full Text] [PDF]

				J. A. Shapiro, W. Huang, C. Zhang, M. J. Hubisz, J. Lu, D. A. Turissini, S. Fang, H.-Y. Wang, R. R. Hudson, R. Nielsen, et al. Adaptive genic evolution in the Drosophila genomes PNAS, February 13, 2007; 104(7): 2271 - 2276. [Abstract] [Full Text] [PDF]

				K. R. Thornton and J. D. Jensen Controlling the False-Positive Rate in Multilocus Genome Scans for Selection Genetics, February 1, 2007; 175(2): 737 - 750. [Abstract] [Full Text] [PDF]

				T. Wiehe, V. Nolte, D. Zivkovic, and C. Schlotterer Identification of Selective Sweeps Using a Dynamically Adjusted Number of Linked Microsatellites Genetics, January 1, 2007; 175(1): 207 - 218. [Abstract] [Full Text] [PDF]

				D. Bachtrog and P. Andolfatto Selection, Recombination and Demographic History in Drosophila miranda Genetics, December 1, 2006; 174(4): 2045 - 2059. [Abstract] [Full Text] [PDF]

				M. Heuertz, E. De Paoli, T. Kallman, H. Larsson, I. Jurman, M. Morgante, M. Lascoux, and N. Gyllenstrand Multilocus Patterns of Nucleotide Diversity, Linkage Disequilibrium and Demographic History of Norway Spruce [Picea abies (L.) Karst] Genetics, December 1, 2006; 174(4): 2095 - 2105. [Abstract] [Full Text] [PDF]

				E. Betran, Y. Bai, and M. Motiwale Fast Protein Evolution and Germ Line Expression of a Drosophila Parental Gene and Its Young Retroposed Paralog Mol. Biol. Evol., November 1, 2006; 23(11): 2191 - 2202. [Abstract] [Full Text] [PDF]

				J. E. Pool and C. F. Aquadro History and Structure of Sub-Saharan Populations of Drosophila melanogaster Genetics, October 1, 2006; 174(2): 915 - 929. [Abstract] [Full Text] [PDF]

				A. D. Cutter, S. E. Baird, and D. Charlesworth High Nucleotide Polymorphism and Rapid Decay of Linkage Disequilibrium in Wild Populations of Caenorhabditis remanei Genetics, October 1, 2006; 174(2): 901 - 913. [Abstract] [Full Text] [PDF]

				H. Quesada, S. E. Ramos-Onsins, J. Rozas, and M. Aguade Positive Selection Versus Demography: Evolutionary Inferences Based on an Unusual Haplotype Structure in Drosophila simulans Mol. Biol. Evol., September 1, 2006; 23(9): 1643 - 1647. [Abstract] [Full Text] [PDF]

				T. M. Panhuis and W. J. Swanson Molecular Evolution and Population Genetic Analysis of Candidate Female Reproductive Genes in Drosophila Genetics, August 1, 2006; 173(4): 2039 - 2047. [Abstract] [Full Text] [PDF]

				P. L. Morrell, D. M. Toleno, K. E. Lundy, and M. T. Clegg Estimating the Contribution of Mutation, Recombination and Gene Conversion in the Generation of Haplotypic Diversity Genetics, July 1, 2006; 173(3): 1705 - 1723. [Abstract] [Full Text] [PDF]

				K. M. Teshima, G. Coop, and M. Przeworski How reliable are empirical genomic scans for selective sweeps? Genome Res., June 1, 2006; 16(6): 702 - 712. [Abstract] [Full Text] [PDF]

				M. T. Hamblin, A. M. Casa, H. Sun, S. C. Murray, A. H. Paterson, C. F. Aquadro, and S. Kresovich Challenges of Detecting Directional Selection After a Bottleneck: Lessons From Sorghum bicolor Genetics, June 1, 2006; 173(2): 953 - 964. [Abstract] [Full Text] [PDF]

				A. J. Greenberg and C.-I Wu Molecular Genetics of Natural Populations Mol. Biol. Evol., May 1, 2006; 23(5): 883 - 886. [Abstract] [Full Text] [PDF]

				P. S. Pennings and J. Hermisson Soft Sweeps II--Molecular Population Genetics of Adaptation from Recurrent Mutation or Migration Mol. Biol. Evol., May 1, 2006; 23(5): 1076 - 1084. [Abstract] [Full Text] [PDF]

				W. Stephan, Y. S. Song, and C. H. Langley The Hitchhiking Effect on Linkage Disequilibrium Between Linked Neutral Loci Genetics, April 1, 2006; 172(4): 2647 - 2663. [Abstract] [Full Text] [PDF]

				K. Thornton and P. Andolfatto Approximate Bayesian Inference Reveals Evidence for a Recent, Severe Bottleneck in a Netherlands Population of Drosophila melanogaster Genetics, March 1, 2006; 172(3): 1607 - 1619. [Abstract] [Full Text] [PDF]

				Y. Kim Allele Frequency Distribution Under Recurrent Selective Sweeps Genetics, March 1, 2006; 172(3): 1967 - 1978. [Abstract] [Full Text] [PDF]

				J. E. Pool, V. B. DuMont, J. L. Mueller, and C. F. Aquadro A Scan of Molecular Variation Leads to the Narrow Localization of a Selective Sweep Affecting Both Afrotropical and Cosmopolitan Populations of Drosophila melanogaster Genetics, February 1, 2006; 172(2): 1093 - 1105. [Abstract] [Full Text] [PDF]

				A. J. Greenberg, J. R. Moran, S. Fang, and C.-I Wu Adaptive Loss of an Old Duplicated Gene During Incipient Speciation Mol. Biol. Evol., February 1, 2006; 23(2): 401 - 410. [Abstract] [Full Text] [PDF]

				S. Beisswanger, W. Stephan, and D. De Lorenzo Evidence for a Selective Sweep in the wapl Region of Drosophila melanogaster Genetics, January 1, 2006; 172(1): 265 - 274. [Abstract] [Full Text] [PDF]

				M. Ashburner and C. M. Bergman Drosophila melanogaster: A case study of a model genomic sequence and its consequences Genome Res., December 1, 2005; 15(12): 1661 - 1667. [Abstract] [Full Text] [PDF]

				K. Thornton Recombination and the Properties of Tajima's D in the Context of Approximate-Likelihood Calculation Genetics, December 1, 2005; 171(4): 2143 - 2148. [Abstract] [Full Text] [PDF]

				V. B. DuMont and C. F. Aquadro Multiple Signatures of Positive Selection Downstream of Notch on the X Chromosome in Drosophila melanogaster Genetics, October 1, 2005; 171(2): 639 - 653. [Abstract] [Full Text] [PDF]

				L. Ometto, S. Glinka, D. De Lorenzo, and W. Stephan Inferring the Effects of Demography and Selection on Drosophila melanogaster Populations from a Chromosome-Wide Scan of DNA Variation Mol. Biol. Evol., October 1, 2005; 22(10): 2119 - 2130. [Abstract] [Full Text] [PDF]