Demography and Natural Selection Have Shaped Genetic Variation in Drosophila melanogaster: A Multi-locus Approach

Corresponding author: David De Lorenzo, Department of Biology II, University of Munich, Luisenstrasse 14, D-80333 Munich, Germany., delorenzo{at}lmu.de (E-mail)

Communicating editor: M. VEUILLE

Demography and selection have been recognized for their important roles in shaping patterns of nucleotide variability. To investigate the relative effects of these forces in the genome of Drosophila melanogaster, we used a multi-locus scan (105 fragments) of X-linked DNA sequence variation in a putatively ancestral African and a derived European population. Surprisingly, we found evidence for a recent size expansion in the African population, i.e., a significant excess of singletons at a chromosome-wide level. In the European population, such an excess was not detected. In contrast to the African population, we found evidence for positive natural selection in the European sample: (i) a large number of loci with low levels of variation and (ii) a significant excess of derived variants at the low-variation loci that are fixed in the European sample but rare in the African population. These results are consistent with the hypothesis that the European population has experienced frequent selective sweeps in the recent past during its adaptation to new habitats. Our study shows the advantages of a genomic approach (over a locus-specific analysis) in disentangling demographic and selective forces.

This article has been cited by other articles:

				N. Svetec, P. Pavlidis, and W. Stephan Recent Strong Positive Selection on Drosophila melanogaster HDAC6, a Gene Encoding a Stress Surveillance Factor, as Revealed by Population Genomic Analysis Mol. Biol. Evol., July 1, 2009; 26(7): 1549 - 1556. [Abstract] [Full Text] [PDF]

				J. Gonzalez, J. M. Macpherson, P. W. Messer, and D. A. Petrov Inferring the Strength of Selection in Drosophila under Complex Demographic Models Mol. Biol. Evol., March 1, 2009; 26(3): 513 - 526. [Abstract] [Full Text] [PDF]

				J. Parsch, Z. Zhang, and J. F. Baines The Influence of Demography and Weak Selection on the McDonald-Kreitman Test: An Empirical Study in Drosophila Mol. Biol. Evol., March 1, 2009; 26(3): 691 - 698. [Abstract] [Full Text] [PDF]

				L.-M. Chevin and F. Hospital Selective Sweep at a Quantitative Trait Locus in the Presence of Background Genetic Variation Genetics, November 1, 2008; 180(3): 1645 - 1660. [Abstract] [Full Text] [PDF]

				D. Zivkovic and T. Wiehe Second-Order Moments of Segregating Sites Under Variable Population Size Genetics, September 1, 2008; 180(1): 341 - 357. [Abstract] [Full Text] [PDF]

				P. R Haddrill and B. Charlesworth Non-neutral processes drive the nucleotide composition of non-coding sequences in Drosophila Biol Lett, August 23, 2008; 4(4): 438 - 441. [Abstract] [Full Text] [PDF]

				J. F. Baines, S. A. Sawyer, D. L. Hartl, and J. Parsch Effects of X-Linkage and Sex-Biased Gene Expression on the Rate of Adaptive Protein Evolution in Drosophila Mol. Biol. Evol., August 1, 2008; 25(8): 1639 - 1650. [Abstract] [Full Text] [PDF]

				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. M. Macpherson, J. Gonzalez, D. M. Witten, J. C. Davis, N. A. Rosenberg, A. E. Hirsh, and D. A. Petrov Nonadaptive Explanations for Signatures of Partial Selective Sweeps in Drosophila Mol. Biol. Evol., June 1, 2008; 25(6): 1025 - 1042. [Abstract] [Full Text] [PDF]

				S. Beisswanger and W. Stephan Evidence that strong positive selection drives neofunctionalization in the tandemly duplicated polyhomeotic genes in Drosophila PNAS, April 8, 2008; 105(14): 5447 - 5452. [Abstract] [Full Text] [PDF]

				A. Riebler, L. Held, and W. Stephan Bayesian Variable Selection for Detecting Adaptive Genomic Differences Among Populations Genetics, March 1, 2008; 178(3): 1817 - 1829. [Abstract] [Full Text] [PDF]

				N. Derome, E. Baudry, D. Ogereau, M. Veuille, and C. Montchamp-Moreau Selective Sweeps in a 2-Locus Model for Sex-Ratio Meiotic Drive in Drosophila simulans Mol. Biol. Evol., February 1, 2008; 25(2): 409 - 416. [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]

				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. Casillas, A. Barbadilla, and C. M. Bergman Purifying Selection Maintains Highly Conserved Noncoding Sequences in Drosophila Mol. Biol. Evol., October 1, 2007; 24(10): 2222 - 2234. [Abstract] [Full Text] [PDF]

				U. Arunyawat, W. Stephan, and T. Stadler Using Multilocus Sequence Data to Assess Population Structure, Natural Selection, and Linkage Disequilibrium in Wild Tomatoes Mol. Biol. Evol., October 1, 2007; 24(10): 2310 - 2322. [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]

				T. L. Turner and M. W. Hahn Locus- and Population-Specific Selection and Differentiation between Incipient Species of Anopheles gambiae Mol. Biol. Evol., September 1, 2007; 24(9): 2132 - 2138. [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]

				S. A. Sawyer, J. Parsch, Z. Zhang, and D. L. Hartl Inaugural Article: Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila PNAS, April 17, 2007; 104(16): 6504 - 6510. [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]

				V. Mustonen and M. Lassig Adaptations to fluctuating selection in Drosophila PNAS, February 13, 2007; 104(7): 2277 - 2282. [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. C. Presgraves and W. Stephan Pervasive Adaptive Evolution among Interactors of the Drosophila Hybrid Inviability Gene, Nup96 Mol. Biol. Evol., January 1, 2007; 24(1): 306 - 314. [Abstract] [Full Text] [PDF]

				P. Pfaffelhuber, B. Haubold, and A. Wakolbinger Approximate Genealogies Under Genetic Hitchhiking Genetics, December 1, 2006; 174(4): 1995 - 2008. [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]

				D. C. Presgraves Intron Length Evolution in Drosophila Mol. Biol. Evol., November 1, 2006; 23(11): 2203 - 2213. [Abstract] [Full Text] [PDF]

				M. Proschel, Z. Zhang, and J. Parsch Widespread Adaptive Evolution of Drosophila Genes With Sex-Biased Expression Genetics, October 1, 2006; 174(2): 893 - 900. [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]

				S. Glinka, D. De Lorenzo, and W. Stephan Evidence of Gene Conversion Associated with a Selective Sweep in Drosophila melanogaster Mol. Biol. Evol., October 1, 2006; 23(10): 1869 - 1878. [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]

				H. Innan Modified Hudson-Kreitman-Aguade Test and Two-Dimensional Evaluation of Neutrality Tests Genetics, July 1, 2006; 173(3): 1725 - 1733. [Abstract] [Full Text] [PDF]

				J. Charlesworth and A. Eyre-Walker The Rate of Adaptive Evolution in Enteric Bacteria Mol. Biol. Evol., July 1, 2006; 23(7): 1348 - 1356. [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]

				E. Baudry, N. Derome, M. Huet, and M. Veuille Contrasted Polymorphism Patterns in a Large Sample of Populations From the Evolutionary Genetics Model Drosophila simulans Genetics, June 1, 2006; 173(2): 759 - 767. [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]

				M. W. Hahn Accurate Inference and Estimation in Population Genomics Mol. Biol. Evol., May 1, 2006; 23(5): 911 - 918. [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]

				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]

				N. Galtier, E. Bazin, and N. Bierne GC-Biased Segregation of Noncoding Polymorphisms in Drosophila Genetics, January 1, 2006; 172(1): 221 - 228. [Abstract] [Full Text] [PDF]

				C. Schlotterer, H. Neumeier, C. Sousa, and V. Nolte Highly Structured Asian Drosophila melanogaster Populations: A New Tool for Hitchhiking Mapping? Genetics, January 1, 2006; 172(1): 287 - 292. [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]

				H. Li and W. Stephan Maximum-Likelihood Methods for Detecting Recent Positive Selection and Localizing the Selected Site in the Genome Genetics, September 1, 2005; 171(1): 377 - 384. [Abstract] [Full Text] [PDF]

				G. Schofl, F. Catania, V. Nolte, and C. Schlotterer African Sequence Variation Accounts for Most of the Sequence Polymorphism in Non-African Drosophila melanogaster Genetics, August 1, 2005; 170(4): 1701 - 1709. [Abstract] [Full Text] [PDF]

				J. M. Braverman, B. P. Lazzaro, M. Aguade, and C. H. Langley DNA Sequence Polymorphism and Divergence at the erect wing and suppressor of sable Loci of Drosophila melanogaster and D. simulans Genetics, July 1, 2005; 170(3): 1153 - 1165. [Abstract] [Full Text] [PDF]

				P. R. Haddrill, K. R. Thornton, B. Charlesworth, and P. Andolfatto Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations Genome Res., June 1, 2005; 15(6): 790 - 799. [Abstract] [Full Text] [PDF]

				T. A. Schlenke and D. J. Begun Linkage Disequilibrium and Recent Selection at Three Immunity Receptor Loci in Drosophila simulans Genetics, April 1, 2005; 169(4): 2013 - 2022. [Abstract] [Full Text] [PDF]

				L. Ometto, W. Stephan, and D. De Lorenzo Insertion/Deletion and Nucleotide Polymorphism Data Reveal Constraints in Drosophila melanogaster Introns and Intergenic Regions Genetics, March 1, 2005; 169(3): 1521 - 1527. [Abstract] [Full Text] [PDF]

				K. J. Schmid, S. Ramos-Onsins, H. Ringys-Beckstein, B. Weisshaar, and T. Mitchell-Olds A Multilocus Sequence Survey in Arabidopsis thaliana Reveals a Genome-Wide Departure From a Neutral Model of DNA Sequence Polymorphism Genetics, March 1, 2005; 169(3): 1601 - 1615. [Abstract] [Full Text] [PDF]

				F. Catania and C. Schlotterer Non-African Origin of a Local Beneficial Mutation in D. melanogaster Mol. Biol. Evol., February 1, 2005; 22(2): 265 - 272. [Abstract] [Full Text] [PDF]

				E. Bazin, L. Duret, S. Penel, and N. Galtier Polymorphix: a sequence polymorphism database Nucleic Acids Res., January 1, 2005; 33(suppl_1): D481 - D484. [Abstract] [Full Text] [PDF]

				J. E. Stajich and M. W. Hahn Disentangling the Effects of Demography and Selection in Human History Mol. Biol. Evol., January 1, 2005; 22(1): 63 - 73. [Abstract] [Full Text] [PDF]

				N. Nikoh, A. Duty, and G. Gibson Effects of Population Structure and Sex on Association Between Serotonin Receptors and Drosophila Heart Rate Genetics, December 1, 2004; 168(4): 1963 - 1974. [Abstract] [Full Text] [PDF]

				A. Das, S. Mohanty, and W. Stephan Inferring the Population Structure and Demography of Drosophila ananassae From Multilocus Data Genetics, December 1, 2004; 168(4): 1975 - 1985. [Abstract] [Full Text] [PDF]

				J. F. Baines, A. Das, S. Mousset, and W. Stephan The Role of Natural Selection in Genetic Differentiation of Worldwide Populations of Drosophila ananassae Genetics, December 1, 2004; 168(4): 1987 - 1998. [Abstract] [Full Text] [PDF]

				E. Sezgin, D. D. Duvernell, L. M. Matzkin, Y. Duan, C.-T. Zhu, B. C. Verrelli, and W. F. Eanes Single-Locus Latitudinal Clines and Their Relationship to Temperate Adaptation in Metabolic Genes and Derived Alleles in Drosophila melanogaster Genetics, October 1, 2004; 168(2): 923 - 931. [Abstract] [Full Text] [PDF]

				J. F. Storz, B. A. Payseur, and M. W. Nachman Genome Scans of DNA Variability in Humans Reveal Evidence for Selective Sweeps Outside of Africa Mol. Biol. Evol., September 1, 2004; 21(9): 1800 - 1811. [Abstract] [Full Text] [PDF]

				D. J. Orengo and M. Aguade Detecting the Footprint of Positive Selection in a European Population of Drosophila melanogaster: Multilocus Pattern of Variation and Distance to Coding Regions Genetics, August 1, 2004; 167(4): 1759 - 1766. [Abstract] [Full Text] [PDF]

				A. Palsson, A. Rouse, R. Riley-Berger, I. Dworkin, and G. Gibson Nucleotide Variation in the Egfr Locus of Drosophila melanogaster Genetics, July 1, 2004; 167(3): 1199 - 1212. [Abstract] [Full Text] [PDF]

				S. Mousset, N. Derome, and M. Veuille A Test of Neutrality and Constant Population Size Based on the Mismatch Distribution Mol. Biol. Evol., April 1, 2004; 21(4): 724 - 731. [Abstract] [Full Text] [PDF]