Mitochondrial data are not suitable for resolving placental mammal phylogeny

Mammalian Genome

Volumn 25, Issue 11-12, 2014, Pages 636-647

  Morgan, Claire C ^a,b   Creevey, Christopher J ^c   O’Connell, Mary J ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

Data quality; Mammal; Mitochondrial DNA; Phylogeny; Site rate categorization; Site stripping

Indexed keywords

AFROTHERIA; ARTICLE; CONTROLLED STUDY; EUARCHONTOGLIRES; GALLUS GALLUS; LAURASIATHERIA; MITOCHONDRIAL GENE; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PLACENTAL MAMMALS; SEQUENCE ALIGNMENT; TAXON; XENARTHRA; ANIMAL; BIOLOGICAL MODEL; DNA SEQUENCE; GENETICS; MAMMAL; MOLECULAR EVOLUTION; MULTILOCUS SEQUENCE TYPING; SPECIES DIFFERENTIATION;

EUTHERIA; MAMMALIA;

MITOCHONDRIAL DNA;

ANIMALS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENETIC SPECIATION; MAMMALS; MODELS, GENETIC; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84912013197     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-014-9544-9     Document Type: Article

References (74)

1. Arnason U, Gullberg A, Janke A, Kullberg M (2007) Mitogenomic analyses of caniform relationships. Mol Phylogenet Evol 45:863–874
2. Awadalla P, Eyre-Walker A, Smith JM (1999) Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science 286:2524–2525
3. Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744
4. 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
5. 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
6. 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
7. 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
8. Caterino MS, Reed RD, Kuo MM, Sperling FA (2001) A partitioned likelihood analysis of swallowtail butterfly phylogeny (Lepidoptera: Papilionidae). Syst Biol 50:106–127
9. Creevey CJ, McInerney JO (2005) Clann: investigating phylogenetic information through supertree analyses. Bioinformatics 21:390–392
10. 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
11. 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
12. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
13. 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
14. 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
15. 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
16. 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
17. Gee H (2003) Evolution: ending incongruence. Nature 425:782
18. 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
19. Hailer F, Leonard JA (2008) Hybridization among three native North American Canis species in a region of natural sympatry. PLoS ONE 3:e3333
20. 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
21. Hebert PD, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321
22. Hedtke SM, Townsend TM, Hillis DM (2006) Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Systematic Biol 55:522–529
23. Hillis DM, Pollock DD, McGuire JA, Zwickl DJ (2003) Is sparse taxon sampling a problem for phylogenetic inference? Syst Biol 52:124–126
24. 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
25. 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
26. Kearney M (2002) Fragmentary taxa, missing data, and ambiguity: mistaken assumptions and conclusions. Syst Biol 51:369–381
27. Kjer KM, Honeycutt RL (2007) Site specific rates of mitochondrial genomes and the phylogeny of eutheria. BMC Evol Biol 7:8
28. Ladoukakis ED, Zouros E (2001) Recombination in animal mitochondrial DNA: evidence from published sequences. Mol Biol Evol 18:2127–2131
29. 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
30. Lunt DH, Hyman BC (1997) Animal mitochondrial DNA recombination. Nature 387:247
31. 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
32. Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730
33. 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
34. Milinkovitch MC, Orti G, Meyer A (1993) Revised phylogeny of whales suggested by mitochondrial ribosomal DNA sequences. Nature 361:346–348
35. 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
36. 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
37. 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
38. 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
39. Myers P, Espinosa R, Parr CS, Jones T, Hammond GS, Dewey TA (2014) The Animal Diversity Web (online). Accessed at http://animaldiversity.org
40. 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
41. 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
42. 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
43. 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
44. Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356:121–125
45. 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
46. Pereira SL (2000) Mitochondrial genome organization and vertebrate phylogenetics. Genet Mol Biol 23:752–754
47. 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
48. 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
49. Phillips MJ, Penny D (2003) The root of the mammalian tree inferred from whole mitochondrial genomes. Mol Phylogenet Evol 28:171–185
50. Pisani D, Benton MJ, Wilkinson M (2007) Congruence of morphological and molecular phylogenies. Acta Biotheor 55:269–281
51. Pollock DD, Zwickl DJ, McGuire JA, Hillis DM (2002) Increased taxon sampling is advantageous for phylogenetic inference. Syst Biol 51:664–671
52. 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
53. Rokas A, Carroll SB (2008) Frequent and widespread parallel evolution of protein sequences. Mol Biol Evol 25:1943–1953
54. 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
55. 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
56. Rosenberg MS, Kumar S (2003) Taxon sampling, bioinformatics, and phylogenomics. Syst Biol 52:119–124
57. 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
58. 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
59. 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
60. 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
61. 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
62. Shen YY, Chen X, Murphy RW (2013) Assessing DNA barcoding as a tool for species identification and data quality control. PLoS ONE 8:e57125
63. Shoshani J, Groves CP, Simons EL, Gunnell GF (1996) Primate phylogeny: morphological vs. molecular results. Mol Phylogenet Evol 5:102–154
64. 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
65. Springer MS, Stanhope MJ, Madsen O, de Jong WW (2004) Molecules consolidate the placental mammal tree. Trends Ecol Evol 19:430–438
66. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
67. 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
68. 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
69. Teeling EC, Hedges SB (2013) Making the impossible possible: rooting the tree of placental mammals. Mol Biol Evol 30:1999–2000
70. 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
71. 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
72. UniProt (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40:D71–D75
73. 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
74. Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Syst Biol 52:528–538