Genomic analysis of European Drosophila melanogaster populations on a dense spatial scale reveals longitudinal population structure and continent-wide selection

80 Genetic variation is the fuel of evolution. However, analyzing dynamics of evolutionary 81 change in natural populations is challenging, genome sequencing of entire populations 82 remains costly and comprehensive sample collection logistically challenging. To tackle this 83 issue and to define relevant spatial and temporal scales of variation for a population 84 genetic model system, the fruit fly Drosophila melanogaster, we have founded the 85 European Drosophila Population Genomics Consortium (DrosEU). Our principal objective 86 is to employ the strengths of this collaborative consortium to extensively sample and 87 sequence natural populations on a continent-wide scale and across distinct timescales. 88 Here we present the first analysis of the first DrosEU pool-sequencing dataset, consisting 89 of 48 population samples collected across the European continent in 2014. The analysis of 90 this comprehensive dataset uncovers novel patterns of variation at multiple levels: 91 genome-wide neutral SNPs, mtDNA haplotypes, inversions and TEs that exhibit previously 92 cryptic longitudinal population structure across the European continent; signatures of 93 selective sweeps shared among the majority of European populations; presumably 94 adaptive clines in inversions; and geographic variation in TEs. Additionally, we document 95 highly variable microbiota among European fruit fly populations and identify several new 96 Drosophila viruses. Our study reveals novel aspects of the population biology of D. 97 melanogaster and illustrates the power of extensive sampling and pooled sequencing of 98 natural populations on a continent-wide scale. 99 100

[1]  Josefa González,et al.  Genome-wide patterns of local adaptation in Western European Drosophila melanogaster natural populations , 2018, Scientific Reports.

[2]  Josefa González,et al.  Genome-wide patterns of local adaptation in Drosophila melanogaster: adding intra European variability to the map , 2018, bioRxiv.

[3]  Meike J. Wittmann,et al.  Seasonally fluctuating selection can maintain polymorphism at many loci via segregation lift , 2017, Proceedings of the National Academy of Sciences.

[4]  M. E. Martino,et al.  Microbial influence on Drosophila biology. , 2017, Current opinion in microbiology.

[5]  Yanhui Hu,et al.  FlyBase at 25: looking to the future , 2016, Nucleic Acids Res..

[6]  J. Pool,et al.  Parallel Evolution of Cold Tolerance within Drosophila melanogaster , 2016, bioRxiv.

[7]  A. Shearer Power and promise , 2016 .

[8]  D. Petrov,et al.  Comparative population genomics of latitudinal variation in Drosophila simulans and Drosophila melanogaster , 2016, Molecular ecology.

[9]  Karen G. Hales,et al.  Genetics on the Fly: A Primer on the Drosophila Model System , 2015, Genetics.

[10]  Ana Conesa,et al.  Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data , 2015, Bioinform..

[11]  Gabor T. Marth,et al.  A global reference for human genetic variation , 2015, Nature.

[12]  J. Pool The Mosaic Ancestry of the Drosophila Genetic Reference Panel and the D. melanogaster Reference Genome Reveals a Network of Epistatic Fitness Interactions , 2015, Molecular biology and evolution.

[13]  Claire L. Webster,et al.  The Discovery, Distribution, and Evolution of Viruses Associated with Drosophila melanogaster , 2015, bioRxiv.

[14]  M. Kapun,et al.  Genomic evidence for role of inversion 3RP of Drosophila melanogaster in facilitating climate change adaptation , 2015, Molecular ecology.

[15]  J. Pool,et al.  Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub‐Saharan Africa , 2015, Journal of evolutionary biology.

[16]  Roger Bivand,et al.  Comparing Implementations of Estimation Methods for Spatial Econometrics , 2015 .

[17]  A. Clark,et al.  Global Diversity Lines–A Five-Continent Reference Panel of Sequenced Drosophila melanogaster Strains , 2015, G3: Genes, Genomes, Genetics.

[18]  B. Charlesworth Causes of natural variation in fitness: Evidence from studies of Drosophila populations , 2015, Proceedings of the National Academy of Sciences.

[19]  R. Newcomb,et al.  Niche construction initiates the evolution of mutualistic interactions. , 2014, Ecology letters.

[20]  C. Schlötterer,et al.  Sequencing pools of individuals — mining genome-wide polymorphism data without big funding , 2014, Nature Reviews Genetics.

[21]  Peter Rodgers,et al.  eulerAPE: Drawing Area-Proportional 3-Venn Diagrams Using Ellipses , 2014, PloS one.

[22]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[23]  Daniel I Bolnick,et al.  Microgeographic adaptation and the spatial scale of evolution. , 2014, Trends in ecology & evolution.

[24]  C. Kent,et al.  Population genomics of the honey bee reveals strong signatures of positive selection on worker traits , 2014, Proceedings of the National Academy of Sciences.

[25]  J. M. Comeron,et al.  The Drosophila early ovarian transcriptome provides insight to the molecular causes of recombination rate variation across genomes , 2013, BMC Genomics.

[26]  Philipp W. Messer,et al.  Population genomics of rapid adaptation by soft selective sweeps. , 2013, Trends in ecology & evolution.

[27]  Kevin R. Thornton,et al.  Abundance and Distribution of Transposable Elements in Two Drosophila QTL Mapping Resources , 2013, Molecular biology and evolution.

[28]  A. Futschik,et al.  A Genome-Wide, Fine-Scale Map of Natural Pigmentation Variation in Drosophila melanogaster , 2013, PLoS genetics.

[29]  James Angus Chandler,et al.  Discovery of Trypanosomatid Parasites in Globally Distributed Drosophila Species , 2013, PloS one.

[30]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[31]  C. Schlötterer,et al.  Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana , 2013, Genome research.

[32]  C. Vogl,et al.  Unconstrained evolution in short introns? – An analysis of genome‐wide polymorphism and divergence data from Drosophila , 2012, Journal of evolutionary biology.

[33]  C. Bergman,et al.  An Age-of-Allele Test of Neutrality for Transposable Element Insertions , 2012, Genetics.

[34]  Russell B. Corbett-Detig,et al.  Population Genomics of Sub-Saharan Drosophila melanogaster: African Diversity and Non-African Admixture , 2012, PLoS genetics.

[35]  Carsten F. Dormann,et al.  Less than eight (and a half) misconceptions of spatial analysis , 2012 .

[36]  Pablo Cingolani,et al.  © 2012 Landes Bioscience. Do not distribute. , 2022 .

[37]  K. Mockaitis,et al.  Ecological Genomics of Anopheles gambiae Along a Latitudinal Cline: A Population-Resequencing Approach , 2012, Genetics.

[38]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[39]  D. Hartl,et al.  Chimeric genes as a source of rapid evolution in Drosophila melanogaster. , 2012, Molecular biology and evolution.

[40]  Robert Kofler,et al.  Sequencing of Pooled DNA Samples (Pool-Seq) Uncovers Complex Dynamics of Transposable Element Insertions in Drosophila melanogaster , 2012, PLoS genetics.

[41]  R. Unckless A DNA Virus of Drosophila , 2011, PloS one.

[42]  Jonathan A. Eisen,et al.  Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host–Microbe Model System , 2011, PLoS genetics.

[43]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[44]  Jan Schröder,et al.  BIOINFORMATICS ORIGINAL PAPER , 2022 .

[45]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[46]  D. Petrov,et al.  Population genomics of transposable elements in Drosophila melanogaster. , 2011, Molecular biology and evolution.

[47]  F. Jiggins,et al.  Trypanosomatids are common and diverse parasites of Drosophila , 2011, Parasitology.

[48]  Bryan D. Kolaczkowski,et al.  Recurrent adaptation in RNA interference genes across the Drosophila phylogeny. , 2011, Molecular biology and evolution.

[49]  B. Charlesworth Molecular population genomics: a short history. , 2010, Genetics research.

[50]  A. Futschik,et al.  The Next Generation of Molecular Markers From Massively Parallel Sequencing of Pooled DNA Samples , 2010, Genetics.

[51]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[52]  M. Goddard,et al.  Copy Number Variation and Transposable Elements Feature in Recent, Ongoing Adaptation at the Cyp6g1 Locus , 2010, PLoS genetics.

[53]  W. Stephan Genetic hitchhiking versus background selection: the controversy and its implications , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Markus Schilhabel,et al.  Nucleotide divergence vs. gene expression differentiation: comparative transcriptome sequencing in natural isolates from the carrion crow and its hybrid zone with the hooded crow , 2010, Molecular ecology.

[55]  W. Stephan,et al.  Recent strong positive selection on Drosophila melanogaster HDAC6, a gene encoding a stress surveillance factor, as revealed by population genomic analysis. , 2009, Molecular biology and evolution.

[56]  R. Durbin,et al.  Mapping Quality Scores Mapping Short Dna Sequencing Reads and Calling Variants Using P

, 2022 .

[57]  J. True,et al.  African Morphology, Behavior and Phermones Underlie Incipient Sexual Isolation between US and Caribbean Drosophila melanogaster , 2008, Evolution; international journal of organic evolution.

[58]  P. Schmidt,et al.  An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster , 2008, Proceedings of the National Academy of Sciences.

[59]  C. Schlötterer,et al.  Contrasting patterns of natural variation in global Drosophila melanogaster populations , 2008, Molecular ecology.

[60]  Josefa González,et al.  High Rate of Recent Transposable Element–Induced Adaptation in Drosophila melanogaster , 2008, PLoS biology.

[61]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[62]  J. True,et al.  Incipient Sexual Isolation Among Cosmopolitan Drosophila Melanogaster Populations , 2008, Evolution; international journal of organic evolution.

[63]  Annalise B. Paaby,et al.  Reproductive Diapause and Life-History Clines in North American Populations of Drosophila melanogaster , 2008, Evolution; international journal of organic evolution.

[64]  M. Stephens,et al.  Interpreting principal component analyses of spatial population genetic variation , 2008, Nature Genetics.

[65]  Minoru Yoshida,et al.  HDAC6 a new cellular stress surveillance factor , 2008, Cell cycle.

[66]  R. Nielsen,et al.  POPULATION SIZE CHANGES RESHAPE GENOMIC PATTERNS OF DIVERSITY , 2007, Evolution; international journal of organic evolution.

[67]  T. McMahon,et al.  Updated world map of the Köppen-Geiger climate classification , 2007 .

[68]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[69]  A. Keller,et al.  Drosophila melanogaster's history as a human commensal , 2007, Current Biology.

[70]  A. Hoffmann,et al.  The association between inversion In(3R)Payne and clinally varying traits in Drosophila melanogaster , 2006, Genetica.

[71]  C. Schlötterer,et al.  Highly Structured Asian Drosophila melanogaster Populations: A New Tool for Hitchhiking Mapping? , 2006, Genetics.

[72]  H. A. Orr,et al.  A Pseudohitchhiking Model of X vs. Autosomal Diversity , 2004, Genetics.

[73]  R. ffrench-Constant,et al.  World‐wide survey of an Accord insertion and its association with DDT resistance in Drosophila melanogaster , 2004, Molecular ecology.

[74]  D. Labuda,et al.  Human X-chromosomal lineages in Europe reveal Middle Eastern and Asiatic contacts , 2004, European Journal of Human Genetics.

[75]  P. Taberlet,et al.  The power and promise of population genomics: from genotyping to genome typing , 2003, Nature Reviews Genetics.

[76]  D. Begun,et al.  Natural selection drives Drosophila immune system evolution. , 2003, Genetics.

[77]  R. ffrench-Constant,et al.  A Single P450 Allele Associated with Insecticide Resistance in Drosophila , 2002, Science.

[78]  P. Andolfatto Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. , 2001, Molecular biology and evolution.

[79]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[80]  T. Jukes,et al.  The neutral theory of molecular evolution. , 2000, Genetics.

[81]  J. Cooper,et al.  Vertebrate Isoforms of Actin Capping Protein β Have Distinct Functions in Vivo , 1999, The Journal of cell biology.

[82]  J. McDonald,et al.  Nucleotide polymorphism at the alcohol dehydrogenase locus of pocket gophers, genus Geomys. , 1998, Molecular biology and evolution.

[83]  Jeffrey R. Powell,et al.  Progress and Prospects in Evolutionary Biology: The Drosophila Model , 1997 .

[84]  Y. Michalakis,et al.  Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. , 1996, Genetics.

[85]  C. Aquadro,et al.  African and North American populations of Drosophila melanogaster are very different at the DNA level , 1993, Nature.

[86]  O. Rieppel Patterns and processes , 1993, Nature.

[87]  C. Aquadro,et al.  Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster , 1992, Nature.

[88]  M. Kreitman,et al.  Adaptive protein evolution at the Adh locus in Drosophila , 1991, Nature.

[89]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[90]  J. David,et al.  Genetic variation of Drosophila melanogaster natural populations. , 1988, Trends in genetics : TIG.

[91]  R. Hudson,et al.  A test of neutral molecular evolution based on nucleotide data. , 1987, Genetics.

[92]  M. Nei Molecular Evolutionary Genetics , 1987 .

[93]  W. Knibb Temporal variation of Drosophila melanogaster Adh allele frequencies, inversion freqencies, and population sizes , 1986, Genetica.

[94]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[95]  P. Menozzi,et al.  Synthetic maps of human gene frequencies in Europeans. , 1978, Science.

[96]  J. Endler Geographic variation, speciation, and clines. , 1977, Monographs in population biology.

[97]  T. Mukai,et al.  Inversion Clines in Populations of DROSOPHILA MELANOGASTER. , 1977, Genetics.

[98]  G. A. Watterson On the number of segregating sites in genetical models without recombination. , 1975, Theoretical population biology.

[99]  R. Levins Evolution in Changing Environments , 1968 .

[100]  L. Cavalli-Sforza Population structure and human evolution , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[101]  P. Moran Notes on continuous stochastic phenomena. , 1950, Biometrika.

[102]  L. Tesfatsion The “Utility” , 1875, Hall's journal of health.

[103]  Christina Freytag,et al.  Textbook On Spherical Astronomy , 2016 .

[104]  C. Lanz,et al.  Population genomics of intrapatient HIV-1 , 2015 .

[105]  H. Ellegren Genome sequencing and population genomics in non-model organisms. , 2014, Trends in ecology & evolution.

[106]  Adrian E. Raftery,et al.  mclust Version 4 for R : Normal Mixture Modeling for Model-Based Clustering , Classification , and Density Estimation , 2012 .

[107]  F. Breden,et al.  Genetic variation in natural populations , 2011 .

[108]  J. Imler,et al.  Drosophila viruses and the study of antiviral host-defense. , 2008, Advances in virus research.

[109]  M. Itoh,et al.  Origin and decay of the P element-associated latitudinal cline in Australian Drosophila melanogaster , 2004, Genetica.

[110]  J. Oakeshott CHROMOSOME INVERSION POLYMORPHISMS IN DROSOPHZLA MELANOGASTER , 2003 .

[111]  R. Lewontin,et al.  The Genetic Basis of Evolutionary Change , 2022 .