Mitonuclear linkage disequilibrium in human populations

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1815, 2015, Pages

  Sloan, Daniel B ^a   Fields, Peter D ^b   Havird, Justin C ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Assisted reproductive technologies; Coevolution; Cytonuclear interactions; Mitochondrial genome; mtDNA; Sex chromosomes

Indexed keywords

ALLELE; CHROMOSOME; COEVOLUTION; DEMOGRAPHIC HISTORY; EPISTASIS; GENE EXPRESSION; GENETIC STRUCTURE; GENOMICS; GENOTYPE; HUMAN EVOLUTION; MITOCHONDRIAL DNA; PROTEIN; PUBLIC HEALTH; RECOMBINATION;

MITOCHONDRIAL DNA;

ALLELE; GENE LINKAGE DISEQUILIBRIUM; GENETICS; HUMAN; HUMAN GENOME; MITOCHONDRION; POPULATION GENETICS; PRINCIPAL COMPONENT ANALYSIS; X CHROMOSOME;

ALLELES; CHROMOSOMES, HUMAN, X; DNA, MITOCHONDRIAL; GENETICS, POPULATION; GENOME, HUMAN; HUMANS; LINKAGE DISEQUILIBRIUM; MITOCHONDRIA; PRINCIPAL COMPONENT ANALYSIS;

EID: 84942064364     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.1704     Document Type: Article

References (102)

1. Rand DM, Haney RA, Fry AJ. 2004 Cytonuclearcoevolution: the genomics of cooperation. TrendsEcol. Evol. 19, 645–653. (doi:10.1016/j.tree.2004.10.003)
2. Levin L, Blumberg A, Barshad G, Mishmar D. 2014Mito-nuclear co-evolution: the positive and negativesides of functional ancient mutations. Front. Genet.5, 448. (doi:10.3389/fgene.2014.00448)
3. Burton RS, Pereira RJ, Barreto FS. 2013 Cytonucleargenomic interactions and hybrid breakdown. Annu.Rev. Ecol. Evol. Syst. 44, 281–302. (doi:10.1146/annurev-ecolsys-110512-135758)
4. Wolff JN, Ladoukakis ED, Enríquez JA, Dowling DK. 2014Mitonuclear interactions: evolutionary consequencesover multiple biological scales. Phil. Trans. R. Soc. B 369,20130443. (doi:10.1098/rstb.2013.0443)
5. Hill GE. 2015 Mitonuclear ecology. Mol. Biol. Evol.32, 1917–1927. (doi:10.1093/molbev/msv104)
6. Gershoni M, Templeton AR, Mishmar D. 2009 Mitochondrial bioenergetics as a major motive forceof speciation. Bioessays 31, 642–650. (doi:10.1002/bies.200800139)
7. Burton RS, Barreto FS. 2012 A disproportionate rolefor mtDNA in Dobzhansky-Muller incompatibilities?Mol. Ecol. 21, 4942–4957. (doi:10.1111/mec.12006)
8. Larsson NG. 2010 Somatic mitochondrial DNAmutations in mammalian aging. Annu. Rev.Biochem. 79, 683–706. (doi:10.1146/annurevbiochem-060408-093701)
9. Tuppen HA, Blakely EL, Turnbull DM, Taylor RW.2010 Mitochondrial DNA mutations and humandisease. Biochim. Biophys. Acta 1797, 113–128.(doi:10.1016/j.bbabio.2009.09.005)
10. Wallace DC, Chalkia D. 2013 Mitochondrial DNAgenetics and the heteroplasmy conundrum inevolution and disease. Cold Spring Harb. Perspect.Med. 3, a021220. (doi:10.1101/cshperspect.a021220)
11. Dowling DK. 2014 Evolutionary perspectives on thelinks between mitochondrial genotype and diseasephenotype. Biochim. Biophys. Acta 1840, 1393–1403. (doi:10.1016/j.bbagen.2013.11.013)
12. Horan MP, Cooper DN. 2014 The emergence of themitochondrial genome as a partial regulator ofnuclear function is providing new insights into thegenetic mechanisms underlying age-relatedcomplex disease. Hum. Genet. 133, 435–458.(doi:10.1007/s00439-013-1402-4)
13. Hudson G et al. 2005 Identification of an Xchromosomallocus and haplotype modulating thephenotype of a mitochondrial DNA disorder.Am. J. Hum. Genet. 77, 1086–1091. (doi:10.1086/498176)
14. Rai E, Sharma S, Koul A, Bhat AK, Bhanwer AJ, Bamezai RN. 2007 Interaction between the UCP2–866G/A, mtDNA 10398G/A and PGC1a p.Thr394Thrand p.Gly482Ser polymorphisms in type 2 diabetessusceptibility in North Indian population. Hum. Genet.122, 535–540. (doi:10.1007/s00439-007-0421-4)
15. Feder J, Ovadia O, Blech I, Cohen J, Wainstein J, Harman-Boehm I, Glaser B, Mishmar D. 2009 Parental diabetes status reveals association ofmitochondrial DNA haplogroup J1 with type 2diabetes. BMC Med. Genet. 10, 60. (doi:10.1186/1471-2350-10-60)
16. Potluri P et al. 2009 A novel NDUFA1 mutationleads to a progressive mitochondrial complex Ispecificneurodegenerative disease. Mol. Genet.Metab. 96, 189–195. (doi:10.1016/j.ymgme.2008.12.004)
17. Bonaiti B, Olsson M, Hellman U, Suhr O, Bonaiti-Pellié C, Planté-Bordeneuve V. 2010 TTR familialamyloid polyneuropathy: does a mitochondrialpolymorphism entirely explain the parent-of-origindifference in penetrance? Eur. J. Hum. Genet. 18,948–952. (doi:10.1038/ejhg.2010.36)
18. Gaweda-Walerych K et al. 2010 Mitochondrialtranscription factor A variants and the risk ofParkinson’s disease. Neurosci. Lett. 469, 24–29.(doi:10.1016/j.neulet.2009.11.037)
19. Taherzadeh-Fard E, Saft C, Akkad DA, Wieczorek S, Haghikia A, Chan A, Epplen JT, Arning L. 2011 PGC-1alpha downstream transcription factors NRF-1 andTFAM are genetic modifiers of Huntington disease.Mol. Neurodegener. 6, 32. (doi:10.1186/1750-1326-6-32)
20. Gomez-Duran A, Pacheu-Grau D, Martinez-Romero I, Lopez-Gallardo E, Lopez-Perez MJ, Montoya J, Ruiz-Pesini E. 2012 Oxidative phosphorylation differencesbetween mitochondrial DNA haplogroups modifythe risk of Leber’s hereditary optic neuropathy.Biochim. Biophys. Acta 1822, 1216–1222. (doi:10.1016/j.bbadis.2012.04.014)
21. Neeve VC et al. 2012 What is influencing thephenotype of the common homozygouspolymerase-gamma mutation p.Ala467Thr? Brain 135, 3614–3626. (doi:10.1093/brain/aws298)
22. Luo LF, Hou CC, Yang WX. 2013 Nuclear factors:roles related to mitochondrial deafness. Gene 520,79–89. (doi:10.1016/j.gene.2013.03.041)
23. Strauss KA et al. 2013 Severity of cardiomyopathyassociated with adenine nucleotide translocator-1deficiency correlates with mtDNA haplogroup. Proc.Natl Acad. Sci. USA 110, 3453–3458. (doi:10.1073/pnas.1300690110)
24. Gershoni M et al. 2014 Disrupting mitochondrialnuclearcoevolution affects OXPHOS complex Iintegrity and impacts human health. Genome Biol.Evol. 6, 2665–2680. (doi:10.1093/gbe/evu208)
25. Kenyon L, Moraes CT. 1997 Expanding thefunctional human mitochondrial DNA database bythe establishment of primate xenomitochondrialcybrids. Proc. Natl Acad. Sci. USA 94, 9131–9135.(doi:10.1073/pnas.94.17.9131)
26. Lin TK, Lin HY, Chen SD, Chuang YC, Chuang JH, Wang PW, Huang ST, Tiao MM, Chen JB, Liou CW.2012 The creation of cybrids harboringmitochondrial haplogroups in the Taiwanesepopulation of ethnic Chinese background: anextensive in vitro tool for the study of mitochondrialgenomic variations. Oxid. Med. Cell. Longev. 2012,824275. (doi:10.1155/2012/824275)
27. Kenney MC et al. 2014 Inherited mitochondrial DNAvariants can affect complement, inflammation andapoptosis pathways: insights into mitochondrialnuclearinteractions. Hum. Mol. Genet. 23,3537–3551. (doi:10.1093/hmg/ddu065)
28. Kenney MC et al. 2014 Molecular and bioenergeticdifferences between cells with African versusEuropean inherited mitochondrial DNA haplogroups:implications for population susceptibility todiseases. Biochim. Biophys. Acta 1842, 208–219.(doi:10.1016/j.bbadis.2013.10.016)
29. Malik D. 2014 Human retinal transmitochondrialcybrids with J or H mtDNA haplogroups responddifferently to ultraviolet radiation: implications forretinal diseases. PLoS ONE 9, e99003. (doi:10.1371/journal.pone.0099003)
30. Couzin-Frankel J. 2015 Eggs’ power plants energizenew IVF debate. Science 348, 14–15. (doi:10.1126/science.348.6230.14)
31. Craven L et al. 2010 Pronuclear transfer in humanembryos to prevent transmission of mitochondrialDNA disease. Nature 465, 82–85. (doi:10.1038/nature08958)
32. Paull D et al. 2013 Nuclear genome transfer inhuman oocytes eliminates mitochondrial DNAvariants. Nature 493, 632–637. (doi:10.1038/nature11800)
33. Tachibana M et al. 2013 Towards germline genetherapy of inherited mitochondrial diseases. Nature493, 627–631. (doi:10.1038/nature11647)
34. Wang T, Sha H, Ji D, Zhang HL, Chen D, Cao Y, Zhu J. 2014 Polar body genome transfer for preventingthe transmission of inherited mitochondrialdiseases. Cell 157, 1591–1604. (doi:10.1016/j.cell.2014.04.042)
35. Wolf DP, Mitalipov N, Mitalipov S. 2015 Mitochondrial replacement therapy in reproductivemedicine. Trends Mol. Med. 21, 68–76. (doi:10.1016/j.molmed.2014.12.001)
36. Reinhardt K, Dowling DK, Morrow EH. 2013 Mitochondrial replacement, evolution, and theclinic. Science 341, 1345–1346. (doi:10.1126/science.1237146)
37. Gemmell N, Wolff JN. 2015 Mitochondrialreplacement therapy: cautiously replace the mastermanipulator. BioEssays 37, 584–585. (doi:10.1002/bies.201500008)
38. Morrow EH, Reinhardt K, Wolff JN, Dowling DK.2015 Risks inherent to mitochondrial replacement.EMBO Rep. 16, 541–544. (doi:10.15252/embr.201439110)
39. Yamaoka M, Isobe K, Shitara H, Yonekawa H, Miyabayashi S, Hayashi JI. 2000 Completerepopulation of mouse mitochondrial DNA-less cellswith rat mitochondrial DNA restores mitochondrialtranslation but not mitochondrial respiratoryfunction. Genetics 155, 301–307.
40. Rand DM, Fry A, Sheldahl L. 2006 Nuclearmitochondrialepistasis and Drosophila aging:introgression of Drosophila simulans mtDNAmodifies longevity in D. melanogaster nuclearbackgrounds. Genetics 172, 329–341. (doi:10.1534/genetics.105.046698)
41. Dowling DK, Friberg U, Hailer F, Arnqvist G. 2007 Intergenomic epistasis for fitness: within-populationinteractions between cytoplasmic and nuclear genesin Drosophila melanogaster. Genetics 175, 235–244. (doi:10.1534/genetics.105.052050)
42. Ellison CK, Burton RS. 2008 Interpopulation hybridbreakdown maps to the mitochondrial genome. Evolution 62, 631–638. (doi:10.1111/j.1558-5646.2007.00305.x)
43. Lee HY, Chou JY, Cheong L, Chang NH, Yang SY, Leu JY. 2008 Incompatibility of nuclear andmitochondrial genomes causes hybrid sterilitybetween two yeast species. Cell 135, 1065–1073.(doi:10.1016/j.cell.2008.10.047)
44. Meiklejohn CD, Holmbeck MA, Siddiq MA, Abt DN, Rand DM, Montooth KL. 2013 An Incompatibilitybetween a mitochondrial tRNA and its nuclearencodedtRNA synthetase compromisesdevelopment and fitness in Drosophila. PLoS Genet.9, e1003238. (doi:10.1371/journal.pgen.1003238)
45. Paliwal S, Fiumera AC, Fiumera HL. 2014 Mitochondrial-nuclear epistasis contributes tophenotypic variation and coadaptation in naturalisolates of Saccharomyces cerevisiae. Genetics 198,1251–1265. (doi:10.1534/genetics.114.168575)
46. Deuse T. 2015 SCNT-derived ESCs with mismatchedmitochondria trigger an immune response inallogeneic hosts. Cell Stem Cell 16, 33–38. (doi:10.1016/j.stem.2014.11.003)
47. Spirek M, Polakova S, Jatzova K, Sulo P. 2015 Postzygoticsterility and cytonuclear compatibility limitsin S. cerevisiae xenomitochondrial cybrids. Front.Genet. 5, 454.
48. Willett CS, Burton RS. 2004 Evolution of interactingproteins in the mitochondrial electron transportsystem in a marine copepod. Mol. Biol. Evol. 21,443–453. (doi:10.1093/molbev/msh031)
49. Mishmar D, Ruiz-Pesini E, Mondragon-Palomino M, Procaccio V, Gaut B, Wallace DC. 2006 Adaptiveselection of mitochondrial complex I subunitsduring primate radiation. Gene 378, 11–18.(doi:10.1016/j.gene.2006.03.015)
50. Osada N, Akashi H. 2012 Mitochondrial-nuclearinteractions and accelerated compensatoryevolution: evidence from the primate cytochrome coxidase complex. Mol. Biol. Evol. 29, 337–346.(doi:10.1093/molbev/msr211)
51. Barreto FS, Burton RS. 2013 Evidence forcompensatory evolution of ribosomal proteins inresponse to rapid divergence of mitochondrial rRNA.Mol. Biol. Evol. 30, 310–314. (doi:10.1093/molbev/mss228)
52. Sloan DB, Triant DA, Wu M, Taylor DR. 2014 Cytonuclear interactions and relaxed selectionaccelerate sequence evolution in organelleribosomes. Mol. Biol. Evol. 31, 673–682. (doi:10.1093/molbev/mst259)
53. Ellison CK, Burton RS. 2010 Cytonuclear conflict ininterpopulation hybrids: the role of RNA polymerase inmtDNA transcription and replication. J. Evol. Biol. 23,528–538. (doi:10.1111/j.1420-9101.2009.01917.x)
54. Burton RS, Ellison CK, Harrison JS. 2006 The sorry stateof F2 hybrids: consequences of rapid mitochondrialDNA evolution in allopatric populations. Am. Nat.168, S14–S24. (doi:10.1086/509046)
55. Asmussen MA, Arnold J. 1991 The effects ofadmixture and population subdivision oncytonuclear disequilibria. Theor. Popul. Biol. 39,273–300. (doi:10.1016/0040-5809(91)90024-A)
56. Wade MJ, Goodnight CJ. 2006 Cyto-nuclear epistasis:two-locus random genetic drift in hermaphroditic anddioecious species. Evolution 60, 643–659. (doi:10.1111/j.0014-3820.2006.tb01146.x)
57. Brandvain Y, Wade MJ. 2009 The functional transferof genes from the mitochondria to the nucleus: theeffects of selection, mutation, population size andrate of self-fertilization. Genetics 182, 1129–1139.(doi:10.1534/genetics.108.100024)
58. Montooth KL, Meiklejohn CD, Abt DN, Rand DM.2010 Mitochondrial-nuclear epistasis affects fitnesswithin species but does not contribute to fixedincompatibilities between species of Drosophila. Evolution 64, 3364–3379. (doi:10.1111/j.1558-5646.2010.01077.x)
59. Fields PD, McCauley DE, McAssey EV, Taylor DR.2014 Patterns of cyto-nuclear linkage disequilibriumin Silene latifolia: genomic heterogeneity andtemporal stability. Heredity 112, 99–104. (doi:10.1038/hdy.2013.79)
60. Li JZ et al. 2008 Worldwide human relationshipsinferred from genome-wide patterns of variation. Science 319, 1100–1104. (doi:10.1126/science.1153717)
61. Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW. 2002 Genetic structure of human populations. Science 298, 2381–2385. (doi:10.1126/science.1078311)
62. Chinnery PF, Craven L, Mitalipov S, Stewart JB, Herbert M, Turnbull DM. 2014 The challenges ofmitochondrial replacement. PLoS Genet. 10,e1004315. (doi:10.1371/journal.pgen.1004315)
63. Ohta T. 1982 Linkage disequilibrium due to randomgenetic drift in finite subdivided populations. Proc.Natl Acad. Sci. USA 79, 1940–1944. (doi:10.1073/pnas.79.6.1940)
64. Nielsen R. 2005 Molecular signatures of naturalselection. Annu. Rev. Genet. 39, 197–218. (doi:10.1146/annurev.genet.39.073003.112420)
65. Wade MJ. 2007 The co-evolutionary genetics ofecological communities. Nat. Rev. Genet. 8,185–195. (doi:10.1038/nrg2031)
66. Reich DE et al. 2001 Linkage disequilibrium in thehuman genome. Nature 411, 199–204. (doi:10.1038/35075590)
67. Ardlie KG, Kruglyak L, Seielstad M. 2002 Patterns oflinkage disequilibrium in the human genome. Nat.Rev. Genet. 3, 299–309. (doi:10.1038/nrg777)
68. International HapMap Consortium. 2003 TheInternational HapMap Project. Nature 426,789–796. (doi:10.1038/nature02168)
69. Conrad DF, Jakobsson M, Coop G, Wen X, Wall JD, Rosenberg NA, Pritchard JK. 2006 A worldwidesurvey of haplotype variation and linkagedisequilibrium in the human genome. Nat. Genet.38, 1251–1260. (doi:10.1038/ng1911)
70. 1000 Genomes Project Consortium. 2012 Anintegrated map of genetic variation from 1,092human genomes. Nature 491, 56–65. (doi:10.1038/nature11632)
71. Wallace DC, Brown MD, Lott MT. 1999 MitochondrialDNA variation in human evolution and disease. Gene 238, 211–230. (doi:10.1016/S0378-1119(99)00295-4)
72. Mishmar D et al. 2003 Natural selection shapedregional mtDNA variation in humans. Proc. NatlAcad. Sci. USA 100, 171–176. (doi:10.1073/pnas.0136972100)
73. Ruiz-Pesini E et al. 2007 An enhanced MITOMAP witha global mtDNA mutational phylogeny. Nucleic AcidsRes. 35, D823–D828. (doi:10.1093/nar/gkl927)
74. Balloux F, Handley LJ, Jombart T, Liu H, Manica A.2009 Climate shaped the worldwide distribution ofhuman mitochondrial DNA sequence variation. Proc. R. Soc. B 276, 3447–3455. (doi:10.1098/rspb.2009.0752)
75. Cann HM et al. 2002 A human genome diversity cellline panel. Science 296, 261–262. (doi:10.1126/science.296.5566.261b)
76. Zhao H, Nettleton D, Soller M, Dekkers JC. 2005 Evaluation of linkage disequilibrium measuresbetween multi-allelic markers as predictors oflinkage disequilibrium between markers and QTL.Genet. Res. 86, 77–87. (doi:10.1017/S001667230500769X)
77. Rosenbloom KR et al. 2015 The UCSC GenomeBrowser database: 2015 update. Nucleic Acids Res.43, D670–D681. (doi:10.1093/nar/gku1177)
78. Chelala C, Khan A, Lemoine NR. 2009 SNPnexus: aweb database for functional annotation of newlydiscovered and public domain single nucleotidepolymorphisms. Bioinformatics 25, 655–661.(doi:10.1093/bioinformatics/btn653)
79. Pagliarini DJ et al. 2008 A mitochondrial proteincompendium elucidates complex I disease biology. Cell 134, 112–123. (doi:10.1016/j.cell.2008.06.016)
80. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N. 1999 Reanalysis andrevision of the Cambridge reference sequence forhuman mitochondrial DNA. Nat. Genet. 23, 147.(doi:10.1038/13779)
81. Kloss-Brandstätter A, Pacher D, Schonherr S, Weissensteiner H, Binna R, Specht G, Kronenberg F.2011 HaploGrep: a fast and reliable algorithm forautomatic classification of mitochondrial DNAhaplogroups. Hum. Mutat. 32, 25–32. (doi:10.1002/humu.21382)
82. van Oven M, Kayser M. 2009 Updatedcomprehensive phylogenetic tree of global humanmitochondrial DNA variation. Hum. Mutat. 30,E386–E394. (doi:10.1002/humu.20921)
83. Patterson N, Price AL, Reich D. 2006 Populationstructure and eigenanalysis. PLoS Genet. 2, e190.(doi:10.1371/journal.pgen.0020190)
84. Purcell S et al. 2007 PLINK: a tool set for wholegenomeassociation and population-based linkageanalyses. Am. J. Hum. Genet. 81, 559–575. (doi:10.1086/519795)
85. Lewontin RC. 1964 The interaction of selection andlinkage. I. General considerations; heterotic models.Genetics 49, 49–67.
86. Hill WG, Robertson A. 1968 Linkage disequilibriumin finite populations. Theor. Appl. Genet. 38, 226–231. (doi:10.1007/BF01245622)
87. R Core Team. 2014 R: a language and environmentfor statistical computing. Vienna, Austria: RFoundation for Statistical Computing.
88. Benjamini Y, Hochberg Y. 1995 Controlling the falsediscovery rate: a practical and powerful approach tomultiple testing. J. R. Stat. Soc. Ser. B Stat.Methodol. 57, 289–300.
89. Huang DW, Sherman BT, Lempicki RA. 2009 Systematic and integrative analysis of large genelists using DAVID bioinformatics resources. Nat.Protoc. 4, 44–57. (doi:10.1038/nprot.2008.211)
90. Drown DM, Preuss KM, Wade MJ. 2012 Evidence ofa paucity of genes that interact with themitochondrion on the X in mammals. Genome Biol.Evol. 4, 763–768. (doi:10.1093/gbe/evs064)
91. Slatkin M. 2008 Linkage disequilibrium:understanding the evolutionary past and mappingthe medical future. Nat. Rev. Genet. 9, 477–485.(doi:10.1038/nrg2361)
92. Neiman M, Taylor DR. 2009 The causes of mutationaccumulation in mitochondrial genomes. Proc. R.Soc. B 276, 1201–1209. (doi:10.1098/rspb.2008.1758)
93. Emery LS, Magnaye KM, Bigham AW, Akey JM, Bamshad MJ. 2015 Estimates of continental ancestryvary widely among individuals with the samemtDNA haplogroup. Am. J. Hum. Genet. 96,183–193. (doi:10.1016/j.ajhg.2014.12.015)
94. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC. 2004 Effects of purifying and adaptiveselection on regional variation in human mtDNA. Science 303, 223–226. (doi:10.1126/science.1088434)
95. Ramachandran S, Rosenberg NA, Zhivotovsky LA, Feldman MW. 2004 Robustness of the inference ofhuman population structure: a comparison ofX-chromosomal and autosomal microsatellites.Hum. Genomics 1, 87–97.
96. Rand DM, Clark AG, Kann LM. 2001 Sexuallyantagonistic cytonuclear fitness interactions inDrosophila melanogaster. Genetics 159, 173–187.
97. Tanaka AJ, Sauer MV, Egli D, Kort DH. 2013 Harnessing the stem cell potential: the path toprevent mitochondrial disease. Nat. Med. 19,1578–1579. (doi:10.1038/nm.3422)
98. Human Fertilisation and Embryology Authority. 2013 HFEA statement regarding the Klaus Reinhardt et al. Science paper ‘Mitochondrial replacement, evolution,and the clinic’. See http://www.hfea.gov.uk/8178.html.
99. Biffi A et al. 2010 Principal-component analysis forassessment of population stratification inmitochondrial medical genetics. Am. J. Hum. Genet.86, 904–917. (doi:10.1016/j.ajhg.2010.05.005)
100. Makowsky R, Yan Q, Wiener HW, Sandel M, Aissani B, Tiwari HK, Shrestha S. 2012 The utility ofmitochondrial and Y chromosome phylogenetic datato improve correction for population stratification.Front. Genet. 3, 301. (doi:10.3389/fgene.2012.00301)
101. Trier CN, Hermansen JS, Saetre GP, Bailey RI.2014 Evidence for mito-nuclear and sex-linkedreproductive barriers between the hybridItalian sparrow and its parent species. PLoSGenet. 10, e1004075. (doi:10.1371/journal.pgen.1004075)
102. Beck EA, Thompson AC, Sharbrough J, Brud E, Llopart A. 2015 Gene flow between Drosophilayakuba and Drosophila santomea in subunit V ofcytochrome c oxidase: a potential case ofcytonuclear co-introgression. Evolution 69, 1973–1986. (doi:10.1111/evo.12718)