期刊论文详细信息
BMC Genomics
Copy number variation in the speciation of pigs: a possible prominent role for olfactory receptors
Martien A M Groenen2  Richard P M A Crooijmans2  Mirte Bosse2  Laurent A F Frantz2  Hendrik-Jan Megens2  Ole Madsen2  Yogesh Paudel1 
[1] Current address: Roche Pharma Research and Early Development, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd, Basel, 4070, Switzerland;Animal Breeding and Genomics Centre, Wageningen University, Wageningen, 6700 AH, The Netherlands
关键词: Read depth method;    Next generation sequencing data;    Copy number variation;    Structural variation;    Speciation;   
Others  :  1177258
DOI  :  10.1186/s12864-015-1449-9
 received in 2014-08-14, accepted in 2015-03-09,  发布年份 2015
PDF
【 摘 要 】

Background

Unraveling the genetic mechanisms associated with reduced gene flow between genetically differentiated populations is key to understand speciation. Different types of structural variations (SVs) have been found as a source of genetic diversity in a wide range of species. Previous studies provided detailed knowledge on the potential evolutionary role of SVs, especially copy number variations (CNVs), between well diverged species of e.g. primates. However, our understanding of their significance during ongoing speciation processes is limited due to the lack of CNV data from closely related species. The genus Sus (pig and its close relatives) which started to diverge ~4 Mya presents an excellent model for studying the role of CNVs during ongoing speciation.

Results

In this study, we identified 1408 CNV regions (CNVRs) across the genus Sus. These CNVRs encompass 624 genes and were found to evolve ~2.5 times faster than single nucleotide polymorphisms (SNPs). The majority of these copy number variable genes are olfactory receptors (ORs) known to play a prominent role in food foraging and mate recognition in Sus. Phylogenetic analyses, including novel Bayesian analysis, based on CNVRs that overlap ORs retain the well-accepted topology of the genus Sus whereas CNVRs overlapping genes other than ORs show evidence for random drift and/or admixture.

Conclusion

We hypothesize that inter-specific variation in copy number of ORs provided the means for rapid adaptation to different environments during the diversification of the genus Sus in the Pliocene. Furthermore, these regions might have acted as barriers preventing massive gene flow between these species during the multiple hybridization events that took place later in the Pleistocene suggesting a possible prominent role of ORs in the ongoing Sus speciation.

【 授权许可】

   
2015 Paudel et al.; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150429022646528.pdf 2550KB PDF download
Figure 5. 29KB Image download
Figure 4. 41KB Image download
Figure 3. 77KB Image download
Figure 2. 45KB Image download
Figure 1. 72KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Mayr E: Animal species and evolution. Animal species and their evolution 1963.
  • [2]Mallet J: A species definition for the modern synthesis. Trends Ecol Evol 1995, 10:294-299.
  • [3]Coyne JA, Orr HA: Speciation. Sinauer Associates Sunderland, MA; 2004.
  • [4]Bolnick DI, Fitzpatrick BM: Sympatric Speciation: Models and Empirical Evidence. Annu Rev Ecol Evol Syst 2007, 38:459-487.
  • [5]Fitzpatrick BM, Fordyce JA, Gavrilets S: What, if anything, is sympatric speciation? J Evol Biol 2008, 21:1452-1459.
  • [6]Niemiller ML, Fitzpatrick BM, Miller BT: Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Mol Ecol 2008, 17:2258-2275.
  • [7]Terai Y, Seehausen O, Sasaki T, Takahashi K, Mizoiri S, Sugawara T, et al.: Divergent Selection on Opsins Drives Incipient Speciation in Lake Victoria Cichlids. PLoS Biol 2006, 4:e433.
  • [8]Ellegren H, Smeds L, Burri R, Olason PI, Backstrom N, Kawakami T, et al.: The genomic landscape of species divergence in Ficedula flycatchers. Nature 2012, 491:756-760.
  • [9]Hearn J, Stone GN, Bunnefeld L, Nicholls JA, Barton NH, Lohse K: Likelihood-based inference of population history from low coverage de novo genome assemblies. Mol Ecol 2013:n/a–n/a.
  • [10]Martin SH, Dasmahapatra KK, Nadeau NJ, Salazar C, Walters JR, Simpson F, et. al: Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research 2013.
  • [11]Lohse K, Frantz LAF: Neandertal Admixture in Eurasia Confirmed by Maximum Likelihood Analysis of Three Genomes. Genetics 2014.
  • [12]Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, et al.: A Draft Sequence of the Neandertal Genome. Science 2010, 328:710-722.
  • [13]Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, et al.: Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 2010, 468:1053-1060.
  • [14]Mitsui Y, Setoguchi H: Demographic histories of adaptively diverged riparian and non-riparian species of Ainsliaea (Asteraceae) inferred from coalescent analyses using multiple nuclear loci. BMC Evol Biol 2012, 12:1-15. BioMed Central Full Text
  • [15]Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J: A Mouse Speciation Gene Encodes a Meiotic Histone H3 Methyltransferase. Science 2009, 323:373-375.
  • [16]Perez DE, Wu CI: Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics 1995, 140:201-206.
  • [17]Masly JP, Jones CD, Noor MAF, Locke J, Orr HA: Gene Transposition as a Cause of Hybrid Sterility in Drosophila. Science 2006, 313:1448-1450.
  • [18]Phadnis N, Orr HA: A Single Gene Causes Both Male Sterility and Segregation Distortion in Drosophila Hybrids. Science 2009, 323:376-379.
  • [19]Turner TL, Hahn MW, Nuzhdin SV: Genomic Islands of Speciation in Anopheles gambiae. PLoS Biol 2005, 3:e285.
  • [20]Noor MAF, Bennett SM: Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 2009, 103:439-444.
  • [21]Michel AP, Sim S, Powell THQ, Taylor MS, Nosil P, Feder JL: Widespread genomic divergence during sympatric speciation. Proc Natl Acad Sci 2010, 107:9724-9729.
  • [22]Vicoso B, Bachtrog D: Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 2013, 499:332-335.
  • [23]Newman TL, Tuzun E, Morrison VA, Hayden KE, Ventura M, McGrath SD, et al.: A genome-wide survey of structural variation between human and chimpanzee. Genome Res 2005, 15:1344-1356.
  • [24]Popesco MC, MacLaren EJ, Hopkins J, Dumas L, Cox M, Meltesen L, et al.: Human Lineage–Specific Amplification, Selection, and Neuronal Expression of DUF1220 Domains. Science 2006, 313:1304-1307.
  • [25]Dumas L, Kim YH, Karimpour-Fard A, Cox M, Hopkins J, Pollack JR, et al.: Gene copy number variation spanning 60 million years of human and primate evolution. Genome Res 2007, 17:1266-1277.
  • [26]Perry GH, Yang F, Marques-Bonet T, Murphy C, Fitzgerald T, Lee AS, et al.: Copy number variation and evolution in humans and chimpanzees. Genome Res 2008, 39:1698-1710.
  • [27]Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA, Nefedov M, et al.: Evolution of Human-Specific Neural SRGAP2 Genes by Incomplete Segmental Duplication. Cell 2012, 149:912-922.
  • [28]Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, et al.: Diet and the evolution of human amylase gene copy number variation. Nat Genet 2007, 39:1256-1260.
  • [29]Nguyen D-Q, Webber C, Hehir-Kwa J, Pfundt R, Veltman J, Ponting CP: Reduced purifying selection prevails over positive selection in human copy number variant evolution. Genome Res 2008, 18:1711-1723.
  • [30]Guerrier S, Coutinho-Budd J, Sassa T, Gresset A, Jordan NV, Chen K, et al.: The F-BAR Domain of srGAP2 Induces Membrane Protrusions Required for Neuronal Migration and Morphogenesis. Cell 2009, 138:990-1004.
  • [31]Frantz L, Schraiber J, Madsen O, Megens H-J, Bosse M, Paudel Y, et al.: Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biol 2013, 14:R107. BioMed Central Full Text
  • [32]Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J: Biodiversity hotspots for conservation priorities. Nature 2000, 403:853-858.
  • [33]Blouch RA, Groves CP: Naturally occurring suid hybrid in Java. Zeitschrift für Säugetierkunde 1990, 55:270-275.
  • [34]Oliver W: The IUCN Red List of Threatened Species. Volume 2014.2; 2008.
  • [35]Sudmant PH, Kitzman JO, Antonacci F, Alkan C, Malig M, Tsalenko A, et al.: Project 1000 Genomes, Eichler EE: Diversity of human copy number variation and multicopy genes. Science 2010, 39:641-646.
  • [36]Bickhart DM, Hou Y, Schroeder SG, Alkan C, Cardone MF, Matukumalli LK, et al.: Copy number variation of individual cattle genomes using next-generation sequencing. Genome res 2012, 22:778-790.
  • [37]Esteve-Codina A, Paudel Y, Ferretti L, Raineri E, Megens H-J, Silio L, et al.: Dissecting structural and nucleotide genome-wide variation in inbred Iberian pigs. BMC Genomics 2013, 14:148. BioMed Central Full Text
  • [38]Paudel Y, Madsen O, Megens H-J, Frantz L, Bosse M, Bastiaansen J, et al.: Evolutionary dynamics of copy number variation in pig genomes in the context of adaptation and domestication. BMC Genomics 2013, 14:449. BioMed Central Full Text
  • [39]Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, et al.: Analyses of pig genomes provide insight into porcine demography and evolution. Nature 2012, 491:393-398.
  • [40]Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, et al.: Ensembl 2012. Nucleic Acids Res 2012, 40:D84-D90.
  • [41]Felsenstein J: PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164–166.
  • [42]Lewis PO: A Likelihood Approach to Estimating Phylogeny from Discrete Morphological Character Data. Systematic Biology 2001, 50:913-925.
  • [43]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
  • [44]Henrichsen CN, Chaignat E, Reymond A: Copy number variants, diseases and gene expression. Human Molecular Genetics 2009, 18:R1-R8.
  • [45]Zhang F, Gu W, Hurles ME, Lupski JR: Copy Number Variation in Human Health, Disease, and Evolution. Annual Review of Genomics and Human Genetics 2009, 10:451-481.
  • [46]Sudmant PH, Huddleston J, Catacchio CR, Malig M, Hillier LW, Baker C, et al.: Great Ape Genome Project, Marques-Bonet T, Eichler EE: Evolution and diversity of copy number variation in the great ape lineage. Genome Research 2013, 23:1373-1382.
  • [47]Liu GE, Hou Y, Zhu B, Cardone MF, Jiang L, Cellamare A, et al.: Analysis of copy number variations among diverse cattle breeds. Genome Res 2010, 20:693-703.
  • [48]Alkan C, Kidd JM, Marques-Bonet T, Aksay G, Antonacci F, Hormozdiari F, et al.: Personalized copy number and segmental duplication maps using next-generation sequencing. Nat Genet 2009, 41:1061-1067.
  • [49]Hach F, Hormozdiari F, Alkan C, Hormozdiari F, Birol I, Eichler EE: Sahinalp SC: mrsFAST: a cache-oblivious algorithm for short-read mapping. Nat Meth 2010, 7:576-577.
  • [50]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al.: 1000 Genome Project Data Processing Subgroup: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
  • [51]Högstrand K, Böhme J: Gene conversion of major histocompatibility complex genes is associated with CpG-rich regions. Immunogenetics 1999, 49:446-455.
  • [52]Galtier N, Piganeau G, Mouchiroud D, Duret L: GC-Content Evolution in Mammalian Genomes: The Biased Gene Conversion Hypothesis. Genetics 2001, 159:907-911.
  • [53]Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, et al.: Accurate whole human genome sequencing using reversible terminator chemistry. Nature 2008, 456:53-59.
  • [54]Dohm JC, Lottaz C, Borodina T, Himmelbauer H. Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Research. 2008;36:e105–5.
  • [55]Aird D, Ross M, Chen W-S, Danielsson M, Fennell T, Russ C, et al.: Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries. Genome Biology 2011, 12:R18. BioMed Central Full Text
  • [56]Benjamini Y, Speed TP. Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Research. 2012;40:e72–2.
  • [57]Oyola S, Otto T, Gu Y, Maslen G, Manske M, Campino S, et al.: Optimizing illumina next-generation sequencing library preparation for extremely at-biased genomes. BMC Genomics 2012, 13:1. BioMed Central Full Text
  • [58]Quail M, Smith M, Coupland P, Otto T, Harris S, Connor T, et al.: A tale of three next generation sequencing platforms: comparison of Ion Torrent Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 2012, 13:341. BioMed Central Full Text
  • [59]Haider S, Ballester B, Smedley D, Zhang J, Rice P, Kasprzyk A: BioMart Central Portal—unified access to biological data. Nucleic Acids Res 2009, 37(suppl 2):W23-W27.
  • [60]Maere S, Heymans K, Kuiper M: BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics 2005, 21:3448-3449.
  • [61]Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al.: Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Research 2003, 13:2498-2504.
  • [62]Fan Y, Wu R, Chen M-H, Kuo L, Lewis PO: Choosing among Partition Models in Bayesian Phylogenetics. Mol Biol Evol 2011, 28:523-532.
  • [63]Xie W, Lewis PO, Fan Y, Kuo L, Chen M-H: Improving Marginal Likelihood Estimation for Bayesian Phylogenetic Model Selection. Systematic Biology 2011, 60:150-160.
  文献评价指标  
  下载次数:58次 浏览次数:21次