Genome‐wide patterns of standing genetic variation in a marine population of three‐spined sticklebacks

Since the end of the Pleistocene, the three‐spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to various freshwater habitats probably originating from ancestral marine populations. Standing genetic variation and the underlying genomic architecture both have been speculated to contribute to recent adaptive radiations of sticklebacks. Here, we expand on the current genomic resources of this fish by providing extensive genome‐wide variation data from six individuals from a marine (North Sea) stickleback population. Using next‐generation sequencing and a combination of paired‐end and mate‐pair libraries, we detected a wide size range of genetic variation. Among the six individuals, we found more than 7% of the genome is polymorphic, consisting of 2 599 111 SNPs, 233 464 indels and structural variation (SV) (>50 bp) such as 1054 copy‐number variable regions (deletions and duplications) and 48 inversions. Many of these polymorphisms affect gene and coding sequences. Based on SNP diversity, we determined outlier regions concordant with signatures expected under adaptive evolution. As some of these outliers overlap with pronounced regions of copy‐number variation, we propose the consideration of such SV when analysing SNP data from re‐sequencing approaches. We further discuss the value of this resource on genome‐wide variation for further investigation upon the relative contribution of standing variation on the parallel evolution of sticklebacks and the importance of the genomic architecture in adaptive radiation.

[1]  Whole genome? , 2015, Nature Genetics.

[2]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

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

[4]  Alex A. Pollen,et al.  The genomic basis of adaptive evolution in threespine sticklebacks , 2012, Nature.

[5]  N. Patrik What is ecological speciation , 2012 .

[6]  W. Cresko,et al.  Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  A. Hendry,et al.  PARALLEL AND NONPARALLEL ASPECTS OF ECOLOGICAL, PHENOTYPIC, AND GENETIC DIVERGENCE ACROSS REPLICATE POPULATION PAIRS OF LAKE AND STREAM STICKLEBACK , 2012, Evolution; international journal of organic evolution.

[8]  Robert D Schnabel,et al.  Copy number variation of individual cattle genomes using next-generation sequencing. , 2012, Genome research.

[9]  D. Absher,et al.  A Genome-wide SNP Genotyping Array Reveals Patterns of Global and Repeated Species-Pair Divergence in Sticklebacks , 2012, Current Biology.

[10]  C. Eizaguirre,et al.  Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations , 2012, Nature Communications.

[11]  C. Doe,et al.  A conserved haplotype controls parallel adaptation in geographically distant salmonid populations , 2012, Molecular ecology.

[12]  Harish Padh,et al.  Implications of gene copy-number variation in health and diseases , 2011, Journal of Human Genetics.

[13]  A. Reymond,et al.  Structural variation and its effect on expression. , 2012, Methods in molecular biology.

[14]  Lin Fang,et al.  Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes , 2011, Nature Biotechnology.

[15]  D. Absher,et al.  Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions , 2012, Proceedings of the Royal Society B: Biological Sciences.

[16]  Xinghua Shi,et al.  Extensive genetic diversity and substructuring among zebrafish strains revealed through copy number variant analysis , 2011, Proceedings of the National Academy of Sciences.

[17]  Paul Stothard,et al.  Whole genome resequencing of black Angus and Holstein cattle for SNP and CNV discovery , 2011, BMC Genomics.

[18]  J. Hedegaard,et al.  Global assessment of genomic variation in cattle by genome resequencing and high-throughput genotyping , 2011, BMC Genomics.

[19]  D. Hartl,et al.  Copy-Number Variation: The Balance between Gene Dosage and Expression in Drosophila melanogaster , 2011, Genome biology and evolution.

[20]  Karsten M. Borgwardt,et al.  Whole-genome sequencing of multiple Arabidopsis thaliana populations , 2011, Nature Genetics.

[21]  Arcadi Navarro,et al.  Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. , 2011, Genome research.

[22]  Thomas M. Keane,et al.  Sequence-based characterization of structural variation in the mouse genome , 2011, Nature.

[23]  Arcadi Navarro,et al.  Gorilla genome structural variation reveals evolutionary parallelisms with chimpanzee. , 2011, Genome research.

[24]  Gonçalo R. Abecasis,et al.  The variant call format and VCFtools , 2011, Bioinform..

[25]  M. Gerstein,et al.  CNVnator: an approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing. , 2011, Genome research.

[26]  J. Merilä,et al.  GLOBAL ANALYSIS OF GENES INVOLVED IN FRESHWATER ADAPTATION IN THREESPINE STICKLEBACKS (GASTEROSTEUS ACULEATUS) , 2011, Evolution; international journal of organic evolution.

[27]  A. Meyer,et al.  Adaptation in the age of ecological genomics: insights from parallelism and convergence. , 2011, Trends in ecology & evolution.

[28]  Ryan E. Mills,et al.  Refinement of primate copy number variation hotspots identifies candidate genomic regions evolving under positive selection , 2011, Genome Biology.

[29]  Bradley P. Coe,et al.  Genome structural variation discovery and genotyping , 2011, Nature Reviews Genetics.

[30]  Ryan E. Mills,et al.  Natural genetic variation caused by small insertions and deletions in the human genome. , 2011, Genome research.

[31]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[32]  P. VanRaden,et al.  Genomic characteristics of cattle copy number variations , 2011, BMC Genomics.

[33]  Kendra J. Lipinski,et al.  High Spontaneous Rate of Gene Duplication in Caenorhabditis elegans , 2011, Current Biology.

[34]  Joshua M. Korn,et al.  Discovery and genotyping of genome structural polymorphism by sequencing on a population scale , 2011, Nature Genetics.

[35]  Todd H. Oakley,et al.  The Ecoresponsive Genome of Daphnia pulex , 2011, Science.

[36]  Bryan D. Kolaczkowski,et al.  Genomic Differentiation Between Temperate and Tropical Australian Populations of Drosophila melanogaster , 2011, Genetics.

[37]  Kenny Q. Ye,et al.  Mapping copy number variation by population scale genome sequencing , 2010, Nature.

[38]  Daniel Rios,et al.  Ensembl 2011 , 2010, Nucleic Acids Res..

[39]  C. Eizaguirre,et al.  Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes , 2011, Evolutionary Ecology.

[40]  J. Slate,et al.  Adaptation genomics: the next generation. , 2010, Trends in ecology & evolution.

[41]  Bo Wang,et al.  Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection , 2010, Nature Genetics.

[42]  R. Faria,et al.  Chromosomal speciation revisited: rearranging theory with pieces of evidence. , 2010, Trends in ecology & evolution.

[43]  Jian Wang,et al.  Genome-wide patterns of genetic variation among elite maize inbred lines , 2010, Nature Genetics.

[44]  Ryan E. Mills,et al.  Small insertions and deletions (INDELs) in human genomes. , 2010, Human molecular genetics.

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

[46]  J. Willis,et al.  A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life-History Transition, Local Adaptation, and Reproductive Isolation , 2010, PLoS biology.

[47]  H. Hoekstra,et al.  Convergence in pigmentation at multiple levels: mutations, genes and function , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Seth Debolt,et al.  Copy Number Variation Shapes Genome Diversity in Arabidopsis Over Immediate Family Generational Scales , 2010, Genome biology and evolution.

[49]  Tomas W. Fitzgerald,et al.  Origins and functional impact of copy number variation in the human genome , 2010, Nature.

[50]  K. Lindblad-Toh,et al.  Whole-genome resequencing reveals loci under selection during chicken domestication , 2010, Nature.

[51]  Ira M. Hall,et al.  Genome-wide mapping and assembly of structural variant breakpoints in the mouse genome. , 2010, Genome research.

[52]  Nicholas Stiffler,et al.  Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags , 2010, PLoS genetics.

[53]  Aaron R. Quinlan,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[54]  Jeremy Schmutz,et al.  Adaptive Evolution of Pelvic Reduction in Sticklebacks by Recurrent Deletion of a Pitx1 Enhancer , 2010, Science.

[55]  Kevin R. Thornton,et al.  Validation of Rearrangement Break Points Identified by Paired-End Sequencing in Natural Populations of Drosophila melanogaster , 2010, Genome biology and evolution.

[56]  Thomas J. Nicholas,et al.  Tracking footprints of artificial selection in the dog genome , 2010, Proceedings of the National Academy of Sciences.

[57]  Yong-shu He,et al.  [Structural variation in the human genome]. , 2009, Yi chuan = Hereditas.

[58]  A. Hendry,et al.  Along the speciation continuum in sticklebacks. , 2009, Journal of fish biology.

[59]  Paul Medvedev,et al.  Computational methods for discovering structural variation with next-generation sequencing , 2009, Nature Methods.

[60]  Xun Xu,et al.  Complete Resequencing of 40 Genomes Reveals Domestication Events and Genes in Silkworm (Bombyx) , 2009, Science.

[61]  Jun Jiang,et al.  Expression regulation and functional characterization of a novel interferon inducible gene Gig2 and its promoter. , 2009, Molecular immunology.

[62]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[63]  M. Hurles,et al.  Copy number variation in human health, disease, and evolution. , 2009, Annual review of genomics and human genetics.

[64]  R. Wilson,et al.  BreakDancer: An algorithm for high resolution mapping of genomic structural variation , 2009, Nature Methods.

[65]  A. Hendry,et al.  Variable Progress Toward Ecological Speciation in Parapatry: Stickleback Across Eight Lake-Stream Transitions , 2009, Evolution; international journal of organic evolution.

[66]  Kai Ye,et al.  Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads , 2009, Bioinform..

[67]  Dolph Schluter,et al.  Genetics and ecological speciation , 2009, Proceedings of the National Academy of Sciences.

[68]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[69]  C. Oosterhout A new theory of MHC evolution: beyond selection on the immune genes , 2009 .

[70]  B. Browning,et al.  A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. , 2009, American journal of human genetics.

[71]  A. Long,et al.  Experimental evolution reveals natural selection on standing genetic variation , 2009, Nature Genetics.

[72]  C. Eizaguirre,et al.  Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. , 2009, Ecology letters.

[73]  C. Eizaguirre,et al.  RSCA genotyping of MHC for high-throughput evolutionary studies in the model organism three-spined stickleback Gasterosteus aculeatus , 2009, BMC Evolutionary Biology.

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

, 2022 .

[75]  Loren H Rieseberg,et al.  Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation? , 2008, Annual review of ecology, evolution, and systematics.

[76]  D. Schluter,et al.  Natural Selection on a Major Armor Gene in Threespine Stickleback , 2008, Science.

[77]  Liangbiao Chen,et al.  Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish , 2008, Proceedings of the National Academy of Sciences.

[78]  J. Merilä,et al.  Identifying footprints of directional and balancing selection in marine and freshwater three‐spined stickleback (Gasterosteus aculeatus) populations , 2008, Molecular ecology.

[79]  Justin O. Borevitz,et al.  Natural Selection Shapes Genome-Wide Patterns of Copy-Number Polymorphism in Drosophila melanogaster , 2008, Science.

[80]  Takanori Nakano,et al.  Reverse Evolution of Armor Plates in the Threespine Stickleback , 2008, Current Biology.

[81]  H. Ellegren,et al.  Genetic basis of fitness differences in natural populations , 2008, Nature.

[82]  H. Hoekstra,et al.  Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits , 2008, Heredity.

[83]  P M Visscher,et al.  A Localized Negative Genetic Correlation Constrains Microevolution of Coat Color in Wild Sheep , 2008, Science.

[84]  D. Schluter,et al.  Adaptation from standing genetic variation. , 2008, Trends in ecology & evolution.

[85]  M. Baerwald,et al.  Discovery of genes implicated in whirling disease infection and resistance in rainbow trout using genome-wide expression profiling , 2008, BMC Genomics.

[86]  C. Peichel,et al.  Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks , 2007, Journal of evolutionary biology.

[87]  Philip M. Kim,et al.  Paired-End Mapping Reveals Extensive Structural Variation in the Human Genome , 2007, Science.

[88]  Fernando A. Villanea,et al.  Diet and the evolution of human amylase gene copy number variation , 2007, Nature Genetics.

[89]  Matthew E Hurles,et al.  The population genetics of structural variation , 2007, Nature Genetics.

[90]  D. Conrad,et al.  Global variation in copy number in the human genome , 2006, Nature.

[91]  Thomas Lengauer,et al.  Improved scoring of functional groups from gene expression data by decorrelating GO graph structure , 2006, Bioinform..

[92]  J. Hermisson,et al.  Soft Sweeps , 2005, Genetics.

[93]  G. Gibson The Synthesis and Evolution of a Supermodel , 2005, Science.

[94]  Jeremy Schmutz,et al.  Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles , 2005, Science.

[95]  H. Rundle,et al.  Ecological speciation: Ecological speciation , 2005 .

[96]  G. Gibson Evolution. The synthesis and evolution of a supermodel. , 2005, Science.

[97]  J. Sikela,et al.  Lineage-Specific Gene Duplication and Loss in Human and Great Ape Evolution , 2004, PLoS biology.

[98]  Kevin Thornton,et al.  libsequence: a C++ class library for evolutionary genetic analysis , 2003, Bioinform..

[99]  N. Barton,et al.  ACCUMULATING POSTZYGOTIC ISOLATION GENES IN PARAPATRY: A NEW TWIST ON CHROMOSOMAL SPECIATION , 2003, Evolution; international journal of organic evolution.

[100]  J. Feder,et al.  Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella. , 2003, Genetics.

[101]  H. Rundle,et al.  Speciation in nature : the threespine stickleback model systems , 2002 .

[102]  K. M. Wegner,et al.  Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity , 2001, Molecular ecology.

[103]  L H. Rieseberg,et al.  Chromosomal rearrangements and speciation. , 2001, Trends in ecology & evolution.

[104]  H. A. Orr,et al.  Haldane's sieve and adaptation from the standing genetic variation. , 2001, Genetics.

[105]  M. Nei,et al.  Evolution by the birth-and-death process in multigene families of the vertebrate immune system. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[106]  D. Schluter Ecological Causes of Adaptive Radiation , 1996, The American Naturalist.

[107]  Dolph Schluter,et al.  Ecological Speciation in Postglacial Fishes , 1996 .

[108]  Susan A. Foster,et al.  The Evolutionary biology of the threespine stickleback , 1995 .

[109]  J. Klein,et al.  The Accordion Model of Mhc Evolution , 1993 .

[110]  K. Isenberg,et al.  Adaptive evolution of G-protein coupled receptor genes. , 1989, Molecular biology and evolution.