Genome-wide analysis in chicken reveals that local levels of genetic diversity are mainly governed by the rate of recombination

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Mugal, Carina F ^a   Nabholz, Benoit ^a,b   Ellegren, Hans ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Chicken; Gene density; Genetic diversity; Mutation; Recombination rate; Selection

Indexed keywords

ARTICLE; ARTIFICIAL SELECTION; BREEDING LINE; BROILER; CHICKEN; DNA BASE COMPOSITION; DOMESTIC ANIMAL; DOMESTICATION; FEMALE; GALLUS GALLUS; GENE LOCUS; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC DISTANCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; MALE; MUTATION RATE; NONHUMAN; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; WILD SPECIES; ANIMAL; BREEDING; GENETIC VARIATION; GENETICS; GENOMICS; REGRESSION ANALYSIS;

ANIMALS; BASE COMPOSITION; BREEDING; CHICKENS; FEMALE; GENETIC VARIATION; GENOMICS; MALE; RECOMBINATION, GENETIC; REGRESSION ANALYSIS;

EID: 84873476826     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-86     Document Type: Article

References (59)

1. Kimura M. Evolutionary rate at the molecular level. Nature 1968, 217(5129):624-626.
2. Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics 1993, 134(4):1289-1303.
3. Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res 1974, 23(1):23-35.
4. Andolfatto P. Adaptive hitchhiking effects on genome variability. Curr Opin Genet Dev 2001, 11(6):635-641.
5. Berry AJ, Ajioka JW, Kreitman M. Lack of polymorphism on the drosophila fourth chromosome resulting from selection. Genetics 1991, 129(4):1111-1117.
6. Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. Melanogaster. Nature 1992, 356(6369):519-520.
7. Nachman MW. Patterns of DNA variability at X-linked loci in Mus domesticus. Genetics 1997, 147(3):1303-1316.
8. Nachman MW, Bauer VL, Crowell SL, Aquadro CF. DNA variability and recombination rates at X-Linked loci in humans. Genetics 1998, 150(3):1133-1141.
9. Hellmann I, Prafer K, Ji H, Zody MC, Pääbo S, Ptak SE. Why do human diversity levels vary at a megabase scale?. Genome Res 2005, 15(9):1222-1231.
10. Spencer CCA, Deloukas P, Hunt S, Mullikin J, Myers S, Silverman B, Donnelly P, Bentley D, McVean G. The influence of recombination on human genetic diversity. PLoS Genetics 2006, 2(9):e148.
11. Cutter AD, Payseur BA. Selection at linked sites in the partial selfer caenorhabditis elegans. Mol Biol Evol 2003, 20(5):665-673.
12. Cutter AD, Choi JY. Natural selection shapes nucleotide polymorphism across the genome of the nematode caenorhabditis briggsae. Genome Res 2010, 20(8):1103-1111.
13. Kraft T, Säll T, Magnusson-Rading I, Nilsson N-O, Halldén C. Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics 1998, 150(3):1239-1244.
14. Dvorák J, Luo M-C, Yang Z-L. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 1998, 148(1):423-434.
15. Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. Mays L.). Proc Natl Acad Sci U S A 2001, 98(16):9161-9166.
16. Lercher MJ, Hurst LD. Human SNP variability and mutation rate are higher in regions of high recombination. Trends in Genetics 2002, 18(7):337-340.
17. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh Y-P, Hahn MW, Nista PM, Jones CD, Kern AD, Dewey CN. Population genomics: whole-genome analysis of polymorphism and divergence in drosophila simulans. PLoS Biology 2007, 5(11):e310.
18. Kulathinal RJ, Bennett SM, Fitzpatrick CL, Noor MAF. Fine-scale mapping of recombination rate in drosophila refines its correlation to diversity and divergence. Proc Natl Acad Sci U S A 2008, 105(29):10051-10056.
19. Huang S-W, Friedman R, Yu N, Yu A, Li W-H. How strong is the mutagenicity of recombination in mammals?. Mol Biol Evol 2005, 22(3):426-431.
20. 1000 GC A map of human genome variation from population-scale sequencing. Nature 2010, 467(7319):1061-1073. 1000 GC.
21. Flowers JM, Molina J, Rubinstein S, Huang P, Schaal BA, Purugganan MD. Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice. Mol Biol Evol 2012, 29(2):675-687.
22. Gossmann TI, Woolfit M, Eyre-Walker A. Quantifying the variation in the effective population size within a genome. Genetics 2011, 189(4):1389-1402.
23. Vigouroux Y, McMullen M, Hittinger CT, Houchins K, Schulz L, Kresovich S, Matsuoka Y, Doebley J. Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc Natl Acad Sci U S A 2002, 99(15):9650-9655.
24. Clark RM, Linton E, Messing J, Doebley JF. Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc Natl Acad Sci U S A 2004, 101(3):700-707.
25. Rubin CJ, Zody MC, Eriksson J, Meadows JR, Sherwood E, Webster MT, Jiang L, Ingman M, Sharpe T, Ka S. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 2010, 464(7288):587-591.
26. Innan H, Kim Y. Pattern of polymorphism after strong artificial selection in a domestication event. Proc Natl Acad Sci U S A 2004, 101(29):10667-10672.
27. ICGSC Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004, 432(7018):695-716. ICGSC.
28. ICPMC A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 2004, 432(7018):717-722. ICPMC.
29. Betancourt AJ, Welch JJ, Charlesworth B. Reduced effectiveness of selection caused by a lack of recombination. Curr Biol 2009, 19(8):655-660.
30. Hodgkinson A, Eyre-Walker A. Variation in the mutation rate across mammalian genomes. Nat Rev Genet 2011, 12(11):756-766.
31. Slotte T, Bataillon T, Hansen TT, St Onge K, Wright SI, Schierup MH. Genomic determinants of protein evolution and polymorphism in Arabidopsis. Genome Biol Evol 2011, 3:1210-1219.
32. Cutter AD, Moses AM. Polymorphism, divergence, and the role of recombination in saccharomyces cerevisiae genome evolution. Mol Biol Evol 2011, 28(5):1745-1754.
33. Payseur BA, Nachman MW. Gene density and human nucleotide polymorphism. Mol Biol Evol 2002, 19(3):336-340.
34. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng HG, Bakker E, Calabrese P, Gladstone J, Goyal R. The pattern of polymorphism in arabidopsis thaliana. PLoS Biology 2005, 3(7):1289-1299.
35. Kawabe A, Forrest A, Wright SI, Charlesworth D. High DNA sequence diversity in pericentromeric genes of the plant arabidopsis lyrata. Genetics 2008, 179(2):985-995.
36. Groenen MAM, Wahlberg P, Foglio M, Cheng HH, Megens H-J, Crooijmans RPMA, Besnier F, Lathrop M, Muir WM, Wong GK-S. A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 2009, 19(3):510-519.
37. Groenen MAM, Cheng HH, Bumstead N, Benkel BF, Briles WE, Burke T, Burt DW, Crittenden LB, Dodgson J, Hillel J. A consensus linkage map of the chicken genome. Genome Res 2000, 10(1):137-147.
38. Huynh LY, Maney DL, Thomas JW. Contrasting population genetic patterns within the white-throated sparrow genome (zonotrichia albicollis). BMC Genet 2010, 11:96.
39. Megens HJ, Crooijmans RPMA, Bastiaansen JWM, Kerstens HHD, Coster A, Jalving R, Vereijken A, Silva P, Muir WM, Cheng HH. Comparison of linkage disequilibrium and haplotype diversity on macro- and microchromosomes in chicken. BMC Genet 2009, 10.
40. Roselius K, Stephan W, Städler T. The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 2005, 171(2):753-763.
41. Axelsson E, Webster MT, Smith NGC, Burt DW, Ellegren H. Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res 2005, 15(1):120-125.
42. Webster MT, Axelsson E, Ellegren H. Strong regional biases in nucleotide substitution in the chicken genome. Mol Biol Evol 2006, 23(6):1203-1216.
43. Duret L, Galtier N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annual Rev Genomics Human Genetics 2009, 10(1):285-311.
44. Hermisson J, Pennings PS. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 2005, 169(4):2335-2352.
45. Granevitze Z, Hillel J, Chen GH, Cuc NTK, Feldman M, Eding H, Weigend S. Genetic diversity within chicken populations from different continents and management histories. Anim Genet 2007, 38(6):576-583.
46. vonHoldt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P, Degenhardt JD, Boyko AR, Earl DA, Auton A. Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 2010, 464(7290):898-902.
47. Amaral AJ, Ferretti L, Megens H-J, Crooijmans RPMA, Nie H, Ramos-Onsins SE, Perez-Enciso M, Schook LB, Groenen MAM. Genome-wide footprints of pig domestication and selection revealed through massive parallel sequencing of pooled DNA. PLoS One 2011, 6(4):e14782.
48. Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glémin S. Grinding up wheat: A massive loss of nucleotide diversity since domestication. Mol Biol Evol 2007, 24(7):1506-1517.
49. Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS. The effects of artificial selection on the maize genome. Science 2005, 308(5726):1310-1314.
50. Fang L, Ye J, Li N, Zhang Y, Li S, Wong G, Wang J. Positive correlation between recombination rate and nucleotide diversity is shown under domestication selection in the chicken genome. Chin Sci Bull 2008, 53(5):746-750.
51. Rao Y, Sun L, Nie Q, Zhang X. The influence of recombination on SNP diversity in chickens. Hereditas 2011, 148(2):63-69.
52. Sundström H, Webster MT, Ellegren H. Reduced variation on the chicken Z chromosome. Genetics 2004, 167:377-385.
53. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, Cline MS, Goldman M, Barber GP, Clawson H, Coelho A. The UCSC genome browser database: update 2011. Nucleic Acids Res 2011, 39(suppl 1):D876-D882.
54. Smedley D, Haider S, Ballester B, Holland R, London D, Thorisson G, Kasprzyk A. BioMart - biological queries made easy. BMC Genomics 2009, 10(1):22.
55. Keightley PD, Gaffney DJ. Functional constraints and frequency of deleterious mutations in noncoding DNA of rodents. Proc Natl Acad Sci U S A 2003, 100(23):13402-13406.
56. Dutheil J, Gaillard S, Bazin E, Glemin S, Ranwez V, Galtier N, Belkhir K. Bio++: a set of C++ libraries for sequence analysis, phylogenetics, molecular evolution and population genetics. BMC Bioinforma 2006, 7(1):188.
57. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17(4):540-552.
58. Abril JF, Castelo R, Guigó R. Comparison of splice sites in mammals and chicken. Genome Res 2005, 15(1):111-119.
59. Naes T, Martens H. Multivariate calibration 2. Chemometric methods. Trac-Trend Anal Chem 1984, 3(10):266-271.