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Mitochondrial data are not suitable for resolving placental mammal phylogeny

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Abstract

Mitochondrial data have traditionally been used in reconstructing a variety of species phylogenies. The low rates of recombination and thorough characterization of mitochondrial data across vertebrate species make it a particularly attractive phylogenetic marker. The relatively low number of fully sequenced mammal genomes and the lack of extensive sampling within Superorders have posed a serious problem for reaching agreement on the placement mammal species. The use of mitochondrial data sequences from large numbers of mammals could serve to circumvent the taxon-sampling deficit. Here we assess the suitability of mitochondrial data as a phylogenetic marker in mammal phylogenetics. MtDNA datasets of mammal origin have been filtered as follows: (i) we have sampled sparsely across the phylogenetic tree, (ii) we have constrained our sampling to genes with high taxon coverage, (iii) we have categorised rates across sites in a phylogeny independent manner and have removed fast evolving sites, and (iv), we have sampled from very shallow divergence times to reduce phylogenetic conflict. However, topologies obtained using these filters are not consistent with previous studies and are discordant across different genes. Individual mitochondrial genes, and indeed all mitochondrial genes analysed as a supermatrix, resulted in poor resolution of the species phylogeny. Overall, our study highlights the limitations of mitochondrial data, not only for resolving deep divergences and but also for shallow divergences in the mammal phylogeny.

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References

  • Arnason U, Gullberg A, Janke A, Kullberg M (2007) Mitogenomic analyses of caniform relationships. Mol Phylogenet Evol 45:863–874

    Article  CAS  PubMed  Google Scholar 

  • Awadalla P, Eyre-Walker A, Smith JM (1999) Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science 286:2524–2525

    Article  CAS  PubMed  Google Scholar 

  • Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Berthier P, Excoffier L, Ruedi M (2006) Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc Biol Sci 273:3101–3109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Branger B, Gillard P, Monrigal C, Thelu S, Robidas E, Viot S, Descamps P, Philippe HJ, Sentilhes L, Winer N (2011) Lessons and impact of two audits on postpartum hemorrhages in 24 maternity hospitals of the network “Securite Naissance - Naitre Ensemble” in “Pays-de-la-Loire” area. J Gynecol Obstet Biol Reprod (Paris) 40:657–667

    Article  CAS  Google Scholar 

  • Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239

    Article  CAS  PubMed  Google Scholar 

  • Campbell LI, Rota-Stabelli O, Edgecombe GD, Marchioro T, Longhorn SJ, Telford MJ, Philippe H, Rebecchi L, Peterson KJ, Pisani D (2011) MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc Natl Acad Sci U S A 108:15920–15924

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Caterino MS, Reed RD, Kuo MM, Sperling FA (2001) A partitioned likelihood analysis of swallowtail butterfly phylogeny (Lepidoptera: Papilionidae). Syst Biol 50:106–127

    Article  CAS  PubMed  Google Scholar 

  • Creevey CJ, McInerney JO (2005) Clann: investigating phylogenetic information through supertree analyses. Bioinformatics 21:390–392

    Article  CAS  PubMed  Google Scholar 

  • Cummins CA, McInerney JO (2011) A method for inferring the rate of evolution of homologous characters that can potentially improve phylogenetic inference, resolve deep divergence and correct systematic biases. Syst Biol 60:833–844

    Article  PubMed  Google Scholar 

  • Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fisher-Reid MC, Wiens JJ (2011) What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Plethodon salamanders and 13 other vertebrate clades. BMC Evol Biol 11:300

    Article  PubMed Central  PubMed  Google Scholar 

  • Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, Gordon L, Hourlier T, Hunt S, Johnson N, Juettemann T, Kahari AK, Keenan S, Kulesha E, Martin FJ, Maurel T, McLaren WM, Murphy DN, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, Ruffier M, Sheppard D, Taylor K, Thormann A, Trevanion SJ, Vullo A, Wilder SP, Wilson M, Zadissa A, Aken BL, Birney E, Cunningham F, Harrow J, Herrero J, Hubbard TJ, Kinsella R, Muffato M, Parker A, Spudich G, Yates A, Zerbino DR, Searle SM (2014) Ensembl 2014. Nucleic Acids Res 42:D749–D755

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frye MS, Hedges SB (1995) Monophyly of the Order Rodentia Inferred from Mitochondrial-DNA Sequences of the Genes for 12 s Ribosomal-Rna, 16 s Ribosomal-Rna, and Transfer-Rna-Valine. Mol Biol Evol 12:168–176

    Article  CAS  PubMed  Google Scholar 

  • Gadagkar SR, Rosenberg MS, Kumar S (2005) Inferring species phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J Exp Zool B Mol Dev Evol 304:64–74

    Article  PubMed  Google Scholar 

  • Gee H (2003) Evolution: ending incongruence. Nature 425:782

    Article  CAS  PubMed  Google Scholar 

  • Gibson A, Gowri-Shankar V, Higgs PG, Rattray M (2005) A comprehensive analysis of mammalian mitochondrial genome base composition and improved phylogenetic methods. Mol Biol Evol 22:251–264

    Article  CAS  PubMed  Google Scholar 

  • Hailer F, Leonard JA (2008) Hybridization among three native North American Canis species in a region of natural sympatry. PLoS ONE 3:e3333

    Article  PubMed Central  PubMed  Google Scholar 

  • Hallstrom BM, Janke A (2008) Resolution among major placental mammal interordinal relationships with genome data imply that speciation influenced their earliest radiations. BMC Evol Biol 8:162

    Article  PubMed Central  PubMed  Google Scholar 

  • Hebert PD, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hedtke SM, Townsend TM, Hillis DM (2006) Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Systematic Biol 55:522–529

    Article  Google Scholar 

  • Hillis DM, Pollock DD, McGuire JA, Zwickl DJ (2003) Is sparse taxon sampling a problem for phylogenetic inference? Syst Biol 52:124–126

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoarau G, Holla S, Lescasse R, Stam WT, Olsen JL (2002) Heteroplasmy and evidence for recombination in the mitochondrial control region of the flatfish Platichthys flesus. Mol Biol Evol 19:2261–2264

    Article  CAS  PubMed  Google Scholar 

  • Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McLnerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29

    Article  PubMed Central  PubMed  Google Scholar 

  • Kearney M (2002) Fragmentary taxa, missing data, and ambiguity: mistaken assumptions and conclusions. Syst Biol 51:369–381

    Article  PubMed  Google Scholar 

  • Kjer KM, Honeycutt RL (2007) Site specific rates of mitochondrial genomes and the phylogeny of eutheria. BMC Evol Biol 7:8

    Article  PubMed Central  PubMed  Google Scholar 

  • Ladoukakis ED, Zouros E (2001) Recombination in animal mitochondrial DNA: evidence from published sequences. Mol Biol Evol 18:2127–2131

    Article  CAS  PubMed  Google Scholar 

  • Lemmon AR, Brown JM, Stanger-Hall K, Lemmon EM (2009) The effect of ambiguous data on phylogenetic estimates obtained by maximum likelihood and Bayesian inference. Syst Biol 58:130–145

    Article  CAS  PubMed  Google Scholar 

  • Lunt DH, Hyman BC (1997) Animal mitochondrial DNA recombination. Nature 387:247

    Article  CAS  PubMed  Google Scholar 

  • Luo A, Zhang A, Ho SY, Xu W, Zhang Y, Shi W, Cameron SL, Zhu C (2011) Potential efficacy of mitochondrial genes for animal DNA barcoding: a case study using eutherian mammals. BMC Genom 12:84

    Article  CAS  Google Scholar 

  • Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730

    Article  CAS  PubMed  Google Scholar 

  • Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334:521–524

    Article  CAS  PubMed  Google Scholar 

  • Milinkovitch MC, Orti G, Meyer A (1993) Revised phylogeny of whales suggested by mitochondrial ribosomal DNA sequences. Nature 361:346–348

    Article  CAS  PubMed  Google Scholar 

  • Morgan CC, Foster PG, Webb AE, Pisani D, McInerney JO, O’Connell MJ (2013) Heterogeneous models place the root of the placental mammal phylogeny. Mol Biol Evol 30:2145–2156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001a) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001b) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W (2007) Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 17:413–421

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Myers P, Espinosa R, Parr CS, Jones T, Hammond GS, Dewey TA (2014) The Animal Diversity Web (online). Accessed at http://animaldiversity.org

  • Nicolas V, Schaeffer B, Missoup AD, Kennis J, Colyn M, Denys C, Tatard C, Cruaud C, Laredo C (2012) Assessment of three mitochondrial genes (16S, Cytb, CO1) for identifying species in the Praomyini tribe (Rodentia: Muridae). PLoS ONE 7:e36586

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nikolaev S, Montoya-Burgos JI, Margulies EH, Rougemont J, Nyffeler B, Antonarakis SE (2007) Early history of mammals is elucidated with the ENCODE multiple species sequencing data. PLoS Genet 3:e2

    Article  PubMed Central  PubMed  Google Scholar 

  • Nishihara H, Hasegawa M, Okada N (2006) Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions. Proc Natl Acad Sci U S A 103:9929–9934

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nishihara H, Maruyama S, Okada N (2009) Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc Natl Acad Sci U S A 106:5235–5240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356:121–125

    Article  CAS  PubMed  Google Scholar 

  • O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, Goldberg SL, Kraatz BP, Luo ZX, Meng J, Ni X, Novacek MJ, Perini FA, Randall ZS, Rougier GW, Sargis EJ, Silcox MT, Simmons NB, Spaulding M, Velazco PM, Weksler M, Wible JR, Cirranello AL (2013) The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339:662–667

    Article  PubMed  Google Scholar 

  • Pereira SL (2000) Mitochondrial genome organization and vertebrate phylogenetics. Genet Mol Biol 23:752–754

    Google Scholar 

  • Philippe H, Snell EA, Bapteste E, Lopez P, Holland PW, Casane D (2004) Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol Biol Evol 21:1740–1752

    Article  CAS  PubMed  Google Scholar 

  • Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Worheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712

    Article  CAS  PubMed  Google Scholar 

  • Phillips MJ, Penny D (2003) The root of the mammalian tree inferred from whole mitochondrial genomes. Mol Phylogenet Evol 28:171–185

    Article  CAS  PubMed  Google Scholar 

  • Pisani D, Benton MJ, Wilkinson M (2007) Congruence of morphological and molecular phylogenies. Acta Biotheor 55:269–281

    Article  PubMed  Google Scholar 

  • Pollock DD, Zwickl DJ, McGuire JA, Hillis DM (2002) Increased taxon sampling is advantageous for phylogenetic inference. Syst Biol 51:664–671

    Article  PubMed Central  PubMed  Google Scholar 

  • Reed RD, Sperling FA (1999) Interaction of process partitions in phylogenetic analysis: an example from the swallowtail butterfly genus Papilio. Mol Biol Evol 16:286–297

    Article  CAS  PubMed  Google Scholar 

  • Rokas A, Carroll SB (2008) Frequent and widespread parallel evolution of protein sequences. Mol Biol Evol 25:1943–1953

    Article  CAS  PubMed  Google Scholar 

  • Romiguier J, Ranwez V, Delsuc F, Galtier N, Douzery EJ (2013) Less is more in mammalian phylogenomics: AT-rich genes minimize tree conflicts and unravel the root of placental mammals. Mol Biol Evol 30:2134–2144

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg MS, Kumar S (2001) Incomplete taxon sampling is not a problem for phylogenetic inference. Proc Natl Acad Sci U S A 98:10751–10756

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rosenberg MS, Kumar S (2003) Taxon sampling, bioinformatics, and phylogenomics. Syst Biol 52:119–124

    Article  PubMed Central  PubMed  Google Scholar 

  • Rota-Stabelli O, Campbell L, Brinkmann H, Edgecombe GD, Longhorn SJ, Peterson KJ, Pisani D, Philippe H, Telford MJ (2011) A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata. Proc Biol Sci 278:298–306

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rubinoff D, Holland BS (2005) Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. Syst Biol 54:952–961

    Article  PubMed  Google Scholar 

  • Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, Kolokotronis SO, Desalle R (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol 7:e20

    Article  PubMed  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  CAS  PubMed  Google Scholar 

  • Shaw KL (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci USA 99:16122–16127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen YY, Chen X, Murphy RW (2013) Assessing DNA barcoding as a tool for species identification and data quality control. PLoS ONE 8:e57125

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shoshani J, Groves CP, Simons EL, Gunnell GF (1996) Primate phylogeny: morphological vs. molecular results. Mol Phylogenet Evol 5:102–154

    Article  CAS  PubMed  Google Scholar 

  • Springer MS, DeBry RW, Douady C, Amrine HM, Madsen O, de Jong WW, Stanhope MJ (2001) Mitochondrial versus nuclear gene sequences in deep-level mammalian phylogeny reconstruction. Mol Biol Evol 18:132–143

    Article  CAS  PubMed  Google Scholar 

  • Springer MS, Stanhope MJ, Madsen O, de Jong WW (2004) Molecules consolidate the placental mammal tree. Trends Ecol Evol 19:430–438

    Article  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A, Auch AF, Meier-Kolthoff J, Goker M (2007) AxPcoords & parallel AxParafit: statistical co-phylogenetic analyses on thousands of taxa. BMC Bioinformatics 8:405

    Article  PubMed Central  PubMed  Google Scholar 

  • Strimmer K, von Haeseler A (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci U S A 94:6815–6819

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Teeling EC, Hedges SB (2013) Making the impossible possible: rooting the tree of placental mammals. Mol Biol Evol 30:1999–2000

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Plewniak F, Ripp R, Thierry JC, Poch O (2001) Towards a reliable objective function for multiple sequence alignments. J Mol Biol 314:937–951

    Article  CAS  PubMed  Google Scholar 

  • Tobe SS, Kitchener AC, Linacre AM (2010) Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome B and cytochrome oxidase subunit I mitochondrial genes. PLoS ONE 5:e14156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • UniProt (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40:D71–D75

    Article  Google Scholar 

  • van Rheede T, Bastiaans T, Boone DN, Hedges SB, de Jong WW, Madsen O (2006) The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and Therians. Mol Biol Evol 23:587–597

    Article  PubMed  Google Scholar 

  • Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Syst Biol 52:528–538

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to thank the Irish Research Council for Science, Engineering and Technology for the Embark Initiative Postgraduate Scholarship to CCM: RS2000172 and Science Foundation Ireland (SFI) for funding to Dr. Mary J. O’Connell (EOB: 2673). We would like to thank the SFI/Higher Education authority (HEA) Irish Centre for High-End Computing (ICHEC: dclif023b) and SCI-SYM DCU for processor time. We would like to thank Paul Kilroy-Glynn for initial discussion, Dr. Davide Pisani and Prof James McInerney for their helpful comments and the Orla Benson travel award (DCU) for funding.

Conflict of interest

Authors declare no conflict of interest.

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Authors and Affiliations

  1. Bioinformatics and Molecular Evolution Group, School of Biotechnology, Dublin City University, Glasnevin, Dublin 9, Ireland

    Claire C. Morgan & Mary J. O’Connell

  2. Centre for Scientific Computing & Complex Systems Modelling (SCI-SYM), Dublin City University, Glasnevin, Dublin 9, Ireland

    Claire C. Morgan & Mary J. O’Connell

  3. National Heart and Lung Institute, Imperial College London, London, W12 0NN, UK

    Claire C. Morgan

  4. Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Wales, UK

    Christopher J. Creevey

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  1. Claire C. Morgan
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Correspondence to Mary J. O’Connell.

Electronic supplementary material

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335_2014_9544_MOESM1_ESM.xls

Supplementary Table 1: Taxon coverage across mtGenes. The species name is given along with whether or not it is represented in each of the 13 mtGenes. The final column shows the total number of times the species is represented across all mtGenes (XLS 93 kb)

335_2014_9544_MOESM2_ESM.nex

Supplementary Table 2: MSA for untreated mtGene and SM datasets. All alignments used in this study are supplied in this file (NEX 4594 kb)

335_2014_9544_MOESM3_ESM.xls

Supplementary Table 3: Phylogenetic trees obtained for all Datasets. The dataset is listed along with the phylogenetic tree and its associated lnL score. The Γ parameter is denoted as +G throughout (XLS 2469 kb)

335_2014_9544_MOESM4_ESM.xls

Supplementary Table 4: Summary of Likelihood Mapping for all Datasets For each dataset, the number of taxa and amino acids are given along with the scores for regions 1–7 from LM analysis. The phylogenetic conflict score is the sum of values from regions 4–7 and this is given in the final column (XLS 95 kb)

Supplementary Table 5: Robinson-Fould distances between topologies (XLS 101 kb)

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Morgan, C.C., Creevey, C.J. & O’Connell, M.J. Mitochondrial data are not suitable for resolving placental mammal phylogeny. Mamm Genome 25, 636–647 (2014). https://doi.org/10.1007/s00335-014-9544-9

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