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Conserved Genetic Architecture Underlying Individual Recombination Rate Variation in a Wild Population of Soay Sheep ( Ovis aries )

Susan E Johnston, Camillo Bérénos, Jon Slate and 1 more

Genetics · 2016

doi:10.1534/genetics.115.185553

Abstract

Meiotic recombination breaks down linkage disequilibrium (LD) and forms new haplotypes, meaning that it is an important driver of diversity in eukaryotic genomes. Understanding the causes of variation in recombination rate is important in interpreting and predicting evolutionary phenomena and in understanding the potential of a population to respond to selection. However, despite attention in model systems, there remains little data on how recombination rate varies at the individual level in natural populations. Here we used extensive pedigree and high-density SNP information in a wild population of Soay sheep (Ovis aries) to investigate the genetic architecture of individual autosomal recombination rates. Individual rates were high relative to other mammal systems and were higher in males than in females (autosomal map lengths of 3748 and 2860 cM, respectively). The heritability of autosomal recombination rate was low but significant in both sexes (h2 = 0.16 and 0.12 in females and males, respectively). In females, 46.7% of the heritable variation was explained by a subtelomeric region on chromosome 6; a genome-wide association study showed the strongest associations at locus RNF212, with further associations observed at a nearby ∼374-kb region of complete LD containing three additional candidate loci, CPLX1, GAK, and PCGF3. A second region on chromosome 7 containing REC8 and RNF212B explained 26.2% of the heritable variation in recombination rate in both sexes. Comparative analyses with 40 other sheep breeds showed that haplotypes associated with recombination rates are both old and globally distributed. Both regions have been implicated in rate variation in mice, cattle, and humans, suggesting a common genetic architecture of recombination rate variation in mammals.

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References 68

1.
Akaike H., 1974 A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19: 716–723.
Not in our library
2.
Aulchenko Y. S. Ripke S. Isaacs A. van Duijn C. M., 2007 GenABEL: an R library for genome-wide association analysis. Bioinformatics 23: 1294–1296.
Not in our library10.1093/bioinformatics/btm108
3.
Genetic Recombination Is Targeted towards Gene Promoter Regions in Dogs · 2013
No notice
4.
Barton N. H., 1998 Why sex and recombination? Science 281: 1986–1990.
Not in our library
5.
Baudat F. Buard J. Grey C. Fledel-Alon A. Ober C., 2010 PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836–840.
Not in our library10.1126/science.1183439
6.
Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches · 2014
No notice
7.
Brandvain Y. Coop G., 2012 Scrambling eggs: meiotic drive and the evolution of female recombination rates. Genetics 190: 709–723.
Not in our library10.1534/genetics.111.136721
8.
Browning S. R. Browning B. L., 2007 Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81: 1084–1097.
Not in our library10.1086/521987
9.
Burt A., 2000 Sex, recombination, and the efficacy of selection: was Weismann right? Evolution 54: 337–351.
Not in our library10.1111/j.0014-3820.2000.tb00038.x
10.
Burt A. Bell G., 1987 Mammalian chiasma frequencies as a test of two theories of recombination. Nature 326: 803–805.
Not in our library10.1038/326803a0
11.
Burt A. Bell G. Harvey P. H., 1991 Sex differences in recombination. J. Evol. Biol. 4: 259–277.
Not in our library
12.
Butler D. G. Cullis B. R. Gilmour A. R. Gogel B. J., 2009 Mixed Models for S Language Environments: ASReml-R Reference Manual. State of Queensland, Department of Primary Industries and Fisheries, Brisbane, Australia.
Not in our library
13.
Charlesworth B. Barton N. H., 1996 Recombination load associated with selection for increased recombination. Genet. Res. Cambr. 67: 27–41.
Not in our library10.1017/s0016672300033450
14.
Clutton-Brock T. Pemberton J. Coulson T. N. Stevenson I. R. MacColl A. D. C., 2004 The sheep of St. Kilda, pp. 17–51 in Soay Sheep: Dynamics and Selection in an Island Population, Vol. 2, edited by Clutton-Brock T. H. Pemberton J. M. Cambridge University Press, Cambridge, UK.
Not in our library
15.
Crow J. F. Kimura M., 1965 Evolution in sexual and asexual populations. Am. Nat. 99: 439–450.
Not in our library
16.
Ensembl 2015 · 2014
No notice
17.
Devlin A. B. Roeder K. Devlin B., 1999 Genomic control for association. Biometrics 55: 997–1004.
Not in our library10.1111/j.0006-341x.1999.00997.x
18.
Dumont B. L. Broman K. W. Payseur B. A., 2009 Variation in genomic recombination rates among heterogeneous stock mice. Genetics 182: 1345–1349.
Not in our library10.1534/genetics.109.105114
19.
Falconer D. S. Mackay T. F. C., 1996 Variance, pp. 122–144 in Introduction to Quantitative Genetics, Ed. 4 Pearson Prentice Hall, Essex, UK.
Not in our library
20.
Felsenstein J., 1974 The evolutionary advantage of recombination. Genetics 78: 737–756.
Not in our library10.1093/genetics/78.2.737
21.
Feulner P. G. D. Gratten J. Kijas J. W. Visscher P. M. Pemberton J. M., 2013 Introgression and the fate of domesticated genes in a wild mammal population. Mol. Ecol. 22: 4210–4221.
Not in our library10.1111/mec.12378
22.
Broad-scale recombination patterns underlying proper disjunction in humans. · 2009
Not checked
23.
Goddard M. E. Hayes B. J., 2009 Genomic selection based on dense genotypes inferred from sparse genotypes. Proc. Assoc. Advmt. Anim. Breed. Genet 18: 26–29.
Not in our library
24.
Green P. Falls K. Crooks S., 1990 Documentation for CRIMAP, Version 2.4. Washington University School of Medicine, St. Louis, MO.
Not in our library
25.
Hassold T. Hunt P., 2001 To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2: 280–291.
Not in our library10.1038/35066065
26.
Henderson C. R., 1975 Best linear unbiased estimation and prediction under a selection model. Biometrics 31: 423–447.
Not in our library
27.
Hill W. G. Robertson A., 1966 The effect of linkage on limits to artificial selection. Genet. Res. 8: 269–294.
Not in our library
28.
Inoue K. Lupski J. R., 2002 Molecular mechanisms for genomic disorders. Ann. Rev. Genomics Hum. Genet. 3: 199–242.
Not in our library10.1146/annurev.genom.3.032802.120023
29.
Jiang Y. Xie M. Chen W. Talbot R. Maddox J. F., 2014 The sheep genome illuminates biology of the rumen and lipid metabolism. Science 344: 1168–1173.
Not in our library10.1126/science.1252806
30.
Johnston S. E. Gratten J. Berenos C. Pilkington J. G. Clutton-Brock T. H., 2013 Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature 502: 93–95.
Not in our library10.1038/nature12489
31.
A Genome Wide Survey of SNP Variation Reveals the Genetic Structure of Sheep Breeds · 2009
No notice
32.
Genome-Wide Analysis of the World's Sheep Breeds Reveals High Levels of Historic Mixture and Strong Recent Selection · 2012
No notice
33.
Koehler K. E. Hawley R. S. Sherman S. Hassold T., 1996 Recombination and nondisjunction in humans and flies. Hum. Mol. Genet. 5: 1495–1504.
Not in our library10.1093/hmg/5.supplement_1.1495
34.
Kong A. Gudbjartsson D. F. Sainz J. Jonsdottir G. M. Gudjonsson S. A., 2002 A high-resolution recombination map of the human genome. Nat. Genet. 31: 241–247.
Not in our library10.1038/ng917
35.
Kong A. Barnard J. Gudbjartsson D. F. Thorleifsson G. Jonsdottir G., 2004 Recombination rate and reproductive success in humans. Nat. Genet. 36: 1203–1206.
Not in our library10.1038/ng1445
36.
Kong A. Thorleifsson G. Stefansson H. Masson G. Helgason A., 2008 Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319: 1398–1401.
Not in our library10.1126/science.1152422
37.
Kong A. Thorleifsson G. Frigge M. L. Masson G. Gudbjartsson D. F., 2014 Common and low-frequency variants associated with genome-wide recombination rate. Nat. Genet. 46: 11–16.
Not in our library10.1038/ng.2833
38.
Recombination Difference between Sexes: A Role for Haploid Selection · 2005
No notice
39.
Li Y. Willer C. J. Ding J. Scheet P. Abecasis G. R., 2010 MaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes. Genet. Epidemiol. 34: 816–834.
Not in our library10.1002/gepi.20533
40.
Cattle Sex-Specific Recombination and Genetic Control from a Large Pedigree Analysis · 2015
No notice

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