Cattle Sex-Specific Recombination and Genetic Control from a Large Pedigree Analysis

PLoS Genetics

Volumn 11, Issue 11, 2015, Pages

  Ma, Li ^a   O'Connell, Jeffrey R ^b   VanRaden, Paul M ^c   Shen, Botong ^a   Padhi, Abinash ^a   Sun, Chuanyu ^d   Bickhart, Derek M ^c   Cole, John B ^c   Null, Daniel J ^c   Liu, George E ^c   Da, Yang ^e   Wiggans, George R ^c  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d National Association of Animal Breeders   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTIFICIAL SELECTION; CHROMOSOME 1; CLINICAL ARTICLE; FEMALE; GENETIC REGULATION; HUMAN; LINKAGE ANALYSIS; MALE; MILK PRODUCTION; PEDIGREE ANALYSIS; SAMPLE SIZE; SEX DIFFERENCE; ANIMAL; BOVINE; CHROMOSOMAL MAPPING; GENETIC RECOMBINATION; GENETICS; PEDIGREE;

ANIMALS; CATTLE; CHROMOSOME MAPPING; FEMALE; MALE; PEDIGREE; RECOMBINATION, GENETIC;

EID: 84949257838     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005387     Document Type: Article

References (72)

1. Stumpf MP, McVean GA, (2003) Estimating recombination rates from population-genetic data. Nature Reviews Genetics 4: 959–968. 14631356
2. Kauppi L, Jeffreys AJ, Keeney S, (2004) Where the crossovers are: recombination distributions in mammals. Nature Reviews Genetics 5: 413–424. 15153994
3. Coop G, Przeworski M, (2006) An evolutionary view of human recombination. Nature Reviews Genetics 8: 23–34. 17146469
4. Paigen K, Petkov P, (2010) Mammalian recombination hot spots: properties, control and evolution. Nature Reviews Genetics 11: 221–233. doi: 10.1038/nrg2712 20168297
5. Lipkin SM, Moens PB, Wang V, Lenzi M, Shanmugarajah D, et al. (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nature genetics 31: 385–390. 12091911
6. Hassold T, Hunt P, (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nature Reviews Genetics 2: 280–291. 11283700
7. Coop G, Myers SR, (2007) Live hot, die young: transmission distortion in recombination hotspots. PLoS genetics 3: e35. 17352536
8. Barton NH, Charlesworth B, (1998) Why sex and recombination? Science 281: 1986–1990. 9748151
9. Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467: 1099–1103. doi: 10.1038/nature09525 20981099
10. Shifman S, Bell JT, Copley RR, Taylor MS, Williams RW, et al. (2006) A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS biology 4: e395. 17105354
11. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836–840. doi: 10.1126/science.1183439 20044539
12. Parvanov ED, Petkov PM, Paigen K, (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835–835. doi: 10.1126/science.1181495 20044538
13. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, et al. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327: 876–879. doi: 10.1126/science.1182363 20044541
14. Jeffreys AJ, Murray J, Neumann R, (1998) High-resolution mapping of crossovers in human sperm defines a minisatellite-associated recombination hotspot. Molecular cell 2: 267–273. 9734365
15. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P, (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321–324. 16224025
16. McVean GA, Myers SR, Hunt S, Deloukas P, Bentley DR, et al. (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304: 581–584. 15105499
17. Pratto F, Brick K, Khil P, Smagulova F, Petukhova GV, et al. (2014) Recombination initiation maps of individual human genomes. Science 346: 1256442. doi: 10.1126/science.1256442 25395542
18. Otto SP, Lenormand T, (2002) Resolving the paradox of sex and recombination. Nature Reviews Genetics 3: 252–261. 11967550
19. Lynn A, Schrump S, Cherry J, Hassold T, Hunt P, (2005) Sex, not genotype, determines recombination levels in mice. The American Journal of Human Genetics 77: 670–675. 16175513
20. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, et al. (2002) A high-resolution recombination map of the human genome. Nature genetics 31: 241–247. 12053178
21. Zenger KR, McKenzie LM, Cooper DW, (2002) The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii). Genetics 162: 321–330. 12242243
22. Marklund L, Moller MJ, Juneja R, Mariani P, Ellegren H, et al. (1996) A comprehensive linkage map of the pig based on a wild pig‐Large White intercross. Animal genetics 27: 255–269. 8856923
23. Maddox JF, Davies KP, Crawford AM, Hulme DJ, Vaiman D, et al. (2001) An enhanced linkage map of the sheep genome comprising more than 1000 loci. Genome research 11: 1275–1289. 11435411
24. Bishop MD, Kappes SM, Keele JW, Stone RT, Sunden S, et al. (1994) A genetic linkage map for cattle. Genetics 136: 619–639. 7908653
25. Barendse W, Armitage S, Kossarek L, Shalom A, Kirkpatrick B, et al. (1994) A genetic linkage map of the bovine genome. Nature genetics 6: 227–235. 8012383
26. Barendse W, Vaiman D, Kemp S, Sugimoto Y, Armitage S, et al. (1997) A medium-density genetic linkage map of the bovine genome. Mammalian Genome 8: 21–28. 9021143
27. Kappes S, Keele JW, Stone RT, McGraw RA, Sonstegard TS, et al. (1997) A second-generation linkage map of the bovine genome. Genome Research 7: 235–249. 9074927
28. Ihara N, Takasuga A, Mizoshita K, Takeda H, Sugimoto M, et al. (2004) A comprehensive genetic map of the cattle genome based on 3802 microsatellites. Genome Research 14: 1987–1998. 15466297
29. Sandor C, Li W, Coppieters W, Druet T, Charlier C, et al. (2012) Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle. PLoS genetics 8: e1002854. doi: 10.1371/journal.pgen.1002854 22844258
30. Weng Z-Q, Saatchi M, Schnabel RD, Taylor JF, Garrick DJ, (2014) Recombination locations and rates in beef cattle assessed from parent-offspring pairs. Genetics Selection Evolution 46: 34.
31. Oliver PL, Goodstadt L, Bayes JJ, Birtle Z, Roach KC, et al. (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS genetics 5: e1000753. doi: 10.1371/journal.pgen.1000753 19997497
32. Zimin AV, Delcher AL, Florea L, Kelley DR, Schatz MC, et al. (2009) A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol 10: R42. doi: 10.1186/gb-2009-10-4-r42 19393038
33. VanRaden P, Null D, Sargolzaei M, Wiggans G, Tooker M, et al. (2013) Genomic imputation and evaluation using high-density Holstein genotypes. Journal of dairy science 96: 668–678. doi: 10.3168/jds.2012-5702 23063157
34. Druet T, Georges M. Pedigree-based haplotype reconstruction, identification of cross-overs and detection of map and genotyping errors using PHASEBOOK; 2014.
35. Garbe J, Da Y, (2003) Locusmap user manual Version 1.1. Department of Animal Science, University of Minnesota, St Paul.
36. Band MR, Larson JH, Rebeiz M, Green CA, Heyen DW, et al. (2000) An ordered comparative map of the cattle and human genomes. Genome research 10: 1359–1368. 10984454
37. Broman KW, Murray JC, Sheffield VC, White RL, Weber JL, (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. The American Journal of Human Genetics 63: 861–869. 9718341
38. Liu EY, Morgan AP, Chesler EJ, Wang W, Churchill GA, et al. (2014) High-resolution sex-specific linkage maps of the mouse reveal polarized distribution of crossovers in male germline. Genetics 197: 91–106. doi: 10.1534/genetics.114.161653 24578350
39. Kong A, Thorleifsson G, Frigge ML, Masson G, Gudbjartsson DF, et al. (2014) Common and low-frequency variants associated with genome-wide recombination rate. Nature genetics 46: 11–16. doi: 10.1038/ng.2833 24270358
40. Yang S-W, Gao C, Chen L, Song Y-L, Zhu J-L, et al. (2012) Nek9 regulates spindle organization and cell cycle progression during mouse oocyte meiosis and its location in early embryo mitosis. Cell Cycle 11: 4366–4377. doi: 10.4161/cc.22690 23159858
41. Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, et al. (2000) MSH4 acts in conjunction with MLH1 during mammalian meiosis. The FASEB Journal 14: 1539–1547. 10928988
42. Ross-Macdonald P, Roeder GS, (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79: 1069–1080. 8001134
43. Eijpe M, Heyting C, Gross B, Jessberger R, (2000) Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes. Journal of Cell Science 113: 673–682. 10652260
44. Ma L, Han S, Yang J, Da Y, (2010) Multi-locus test conditional on confirmed effects leads to increased power in genome-wide association studies. PloS one 5: e15006. doi: 10.1371/journal.pone.0015006 21103364
45. Liu Y, Qin X, Song X-ZH, Jiang H, Shen Y, et al. (2009) Bos taurus genome assembly. BMC genomics 10: 180. doi: 10.1186/1471-2164-10-180 19393050
46. Muñoz-Fuentes V, Marcet-Ortega M, Alkorta-Aranburu G, Forsberg CL, Morrell JM, et al. (2015) Strong artificial selection in domestic mammals did not result in an increased recombination rate. Molecular biology and evolution 32: 510–523. doi: 10.1093/molbev/msu322 25414125
47. Hayes B, Bowman P, Chamberlain A, Goddard M, (2009) Invited review: Genomic selection in dairy cattle: Progress and challenges. Journal of dairy science 92: 433–443. doi: 10.3168/jds.2008-1646 19164653
48. VanRaden P, Van Tassell C, Wiggans G, Sonstegard T, Schnabel R, et al. (2009) Invited Review: Reliability of genomic predictions for North American Holstein bulls. Journal of Dairy Science 92: 16–24. doi: 10.3168/jds.2008-1514 19109259
49. Sodeland M, Kent M, Hayes BJ, Grove H, Lien S, (2011) Recent and historical recombination in the admixed Norwegian Red cattle breed. BMC genomics 12: 33. doi: 10.1186/1471-2164-12-33 21232164
50. Pál C, Papp B, Hurst LD, (2001) Does the recombination rate affect the efficiency of purifying selection? The yeast genome provides a partial answer. Molecular biology and evolution 18: 2323–2326. 11719582
51. Lenormand T, Dutheil J, (2005) Recombination difference between sexes: a role for haploid selection. PLoS biology 3: e63. 15736976
52. Dumont BL, Payseur BA, (2011) Genetic analysis of genome-scale recombination rate evolution in house mice. PLoS genetics 7: e1002116. doi: 10.1371/journal.pgen.1002116 21695226
53. Murdoch B, Owen N, Shirley S, Crumb S, Broman KW, et al. (2010) Multiple loci contribute to genome-wide recombination levels in male mice. Mammalian Genome 21: 550–555. doi: 10.1007/s00335-010-9303-5 21113599
54. Decker JE, McKay SD, Rolf MM, Kim J, Alcalá AM, et al. (2014) Worldwide patterns of ancestry, divergence, and admixture in domesticated cattle. PLoS genetics 10: e1004254. doi: 10.1371/journal.pgen.1004254 24675901
55. Butlin RK, (2005) Recombination and speciation. Molecular Ecology 14: 2621–2635. 16029465
56. Ross‐Ibarra J, (2004) The evolution of recombination under domestication: a test of two hypotheses. The American Naturalist 163: 105–112. 14767840
57. Burt A, Bell G, (1987) Mammalian chiasma frequencies as a test of two theories of recombination. Nature 326: 803–805. 3574451
58. Maddox JF, Cockett NE, (2007) An update on sheep and goat linkage maps and other genomic resources. Small ruminant research 70: 4–20.
59. Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F, et al. (2009) Revealing the history of sheep domestication using retrovirus integrations. Science 324: 532–536. doi: 10.1126/science.1170587 19390051
60. Poissant J, Hogg JT, Davis CS, Miller JM, Maddox JF, et al. (2010) Genetic linkage map of a wild genome: genomic structure, recombination and sexual dimorphism in bighorn sheep. BMC genomics 11: 524. doi: 10.1186/1471-2164-11-524 20920197
61. Arias JA, Keehan M, Fisher P, Coppieters W, Spelman R, (2009) A high density linkage map of the bovine genome. BMC genetics 10: 18. doi: 10.1186/1471-2156-10-18 19393043
62. Groenen MA, Wahlberg P, Foglio M, Cheng HH, Megens H-J, et al. (2009) A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Research 19: 510–519. doi: 10.1101/gr.086538.108 19088305
63. Lucy M, (2001) Reproductive loss in high-producing dairy cattle: where will it end? Journal of dairy science 84: 1277–1293. 11417685
64. Pryce J, Royal M, Garnsworthy P, Mao IL, (2004) Fertility in the high-producing dairy cow. Livestock Production Science 86: 125–135.
65. Wiggans G, Cooper T, Null D, VanRaden P Increasing the Number of Single Nucleotide Polymorphisms Used in Genomic Evaluations of Dairy Cattle.
66. Druet T, Georges M, (2010) A hidden Markov model combining linkage and linkage disequilibrium information for haplotype reconstruction and quantitative trait locus fine mapping. Genetics 184: 789–798. doi: 10.1534/genetics.109.108431 20008575
67. Zhao H, Speed TP, (1996) On genetic map functions. Genetics 142: 1369–1377. 8846913
68. Haldane J, (1919) The combination of linkage values and the calculation of distances between the loci of linked factors. Journal of Genetics 8: 299–939.
69. R Core Team R (2014) R: A language and environment for statistical computing.
70. VanRaden PM, O’Connell JR, Wiggans GR, Weigel KA, (2011) Genomic evaluations with many more genotypes. Genet Sel Evol 43.
71. O’Connell JR (2014) MMAP User Guide (2014). http://ednsomumarylandedu/mmap/indexphp.
72. O'Connell J (2013) MMAP: a comprehensive mixed model program for analysis of pedigree and population data. 63th Annual Meeting of The American Society of Human Genetics, Oct 22–262013, Boston, USA.