Molecular decay of the tooth gene enamelin (ENAM) mirrors the loss of enamel in the fossil record of placental mammals

PLoS Genetics

Volumn 5, Issue 9, 2009, Pages

  Meredith, Robert W ^a   Gatesy, John ^a   Murphy, William J ^b   Ryder, Oliver A ^c   Springer, Mark S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c INSTITUTE FOR CONSERVATION RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DANIAN; ENAMEL; ENAMELIN GENE; EOCENE; EVOLUTION; FOSSIL; FRAMESHIFT MUTATION; GENE; MAMMAL; MIDDLE MIOCENE; MOLECULAR CLOCK; MOLECULAR EVOLUTION; NONHUMAN; OLIGOCENE; PHYLOGENY; PSEUDOGENE; STOP CODON; ANIMAL; CHEMISTRY; CLASSIFICATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

CETACEA; DASYPODIDAE; EUTHERIA; MYRMECOPHAGIDAE; ORYCTEROPODIDAE; PHOLIDOTA (MAMMAL); SLOTHS; TUBULIDENTATA; XENARTHRA;

ENAMEL PROTEIN; TUFTELIN;

ANIMALS; BASE SEQUENCE; DENTAL ENAMEL; DENTAL ENAMEL PROTEINS; EVOLUTION, MOLECULAR; FOSSILS; MAMMALS; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; SEQUENCE ALIGNMENT;

EID: 70349668982     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000634     Document Type: Article

References (76)

1. Futuyma DJ (1998) Evolutionary biology. Sunderland: Sinauer.
2. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray.
3. Darwin C (1871) The descent of man, and selection in relation to sex. London: John Murray.
4. Bedjer L, Hall BK (2002) Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss. Evol Dev 4: 445-458.
5. Fong DW, Kane TC, Culver DC (1995) Vestigialization and loss of nonfunctional characters. Annu Rev Ecol Syst 26: 249-268.
6. Nishikimi M, Fukuyama R, Minoshima S, Shimizu N, Yagi K (1994) Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-γ- clactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J Biol Chem 269: 13685-13688. (Pubitemid 24978639)
7. Ohta Y, Nishikimi M (1999) Random nucleotide substitutions in primate nonfunctional gene for L-gulono-c-lactone oxidase, the missing enzyme in Lascorbic acid biosynthesis. Biochim Biophys Acta 1472: 408-411. (Pubitemid 29486553)
8. Hu JC-C, Chun Y-HP, Al Hazzazzi T, Simmer JP (2007) Enamel formation and amelogenesis imperfecta. Cells Tissues Organs 186: 78-85.
9. Wright JT, Hart TC, Hart PS, Simmons D, Suggs C, et al. (2009) Human and mouse enamel phenotypes resulting from mutation or altered expression of AMEL, ENAM, MMP20 and KLK4. Cells Tissues Organs 189: 224-229.
10. Kawasaki K, Weiss KM (2003) Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci U S A 100: 4060-4065. (Pubitemid 36418157)
11. Sire J-Y, Davit-Beal T, Delgado S, Gu X (2007) The origin and evolution of enamel mineralization genes. Cells Tissues Organs 186: 25-48. (Pubitemid 47026715)
12. Kawasaki K (2009) The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues. Dev Genes Evol 219: 147-157.
13. Hu C-C, Fukae M, Uchida T, Qian Q, Zhang CH, et al. (1997) Cloning and characterization of porcine enamelin mRNAs. J Dent Res 76: 1720-1729. (Pubitemid 127732194)
14. Hu JC-C, Hu Y, Smith CE, McKee MD, Wright JT, et al. (2008) Enamel defects and ameloblast-specific expression in Enam knock-out/lacZ knock-in mice. J Biol Chem 283: 10858-10871.
15. Deméré TA, McGowen MR, Berta A, Gatesy J (2008) Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst Biol 57: 15-37.
16. Osborn HF (1893) Recent researches upon the succession of teeth in mammals. Amer Nat 27: 493-508.
17. Spurgin AM (1904) Enamel in the teeth of an embryo edentate (Dasypus novemcinctus Linn). Amer J Anat 3: 75-84.
18. Murphy WJ, Eizirik E, O'Brien SJ, Madsen O, Scally M, et al. (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348-2351. (Pubitemid 33140557)
19. Springer MS, Burk-Herrick A, Meredith R, Eizirik E, Teeling E, et al. (2007) The adequacy of morphology for reconstructing the early history of placental mammals. Syst Biol 56: 673-684.
20. Delsuc F, Vizcaino SF, Douzery EJP (2004) Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans. BMC Evol Biol 4: 11. (Pubitemid 38761940)
21. O'Leary MA, Gatesy J (2008) Impact of increased character sampling on the phylogeny of Cetartiodactyla (Mammalia): combined analysis including fossils. Cladistics 24: 397-442.
22. Holroyd PA, Mussell JC (2005) Macroscelidea and Tubulidentata. In: Rose KD, Archibald JD, eds. The rise of placental mammals. Baltimore: The Johns Hopkins Univ Press. pp 71-83.
23. Murphy WJ, Eizirik E (2009) Placental mammals (Eutheria). In: Hedges SB, Kumar S, eds. The timetree of life. Oxford: Oxford Univ Press. pp 471-474.
24. Patterson B (1975) The fossil aardvarks (Mammalia: Tubulidentata). Bull Mus Comp Zool 147: 185-237.
25. Milledge S (2003) Fossil aardvarks from the Lothagam beds. In: Leakey J, Harris J, eds. Lothagam: The dawn of humanity in Eastern Africa. New York: Columbia University Press. pp 363-368.
26. Wolfe KH, Sharp PM, Li W-H (1989) Mutation rates differ among regions of the mammalian genome. Nature 337: 283-285.
27. Kumar S, Subramanian S (2002) Mutation rates in mammalian genomes. Proc Natl Acad Sci U S A 99: 803-808.
28. Bustamante CD, Nielsen R, Hartl DL (2002) A maximum likelihood method analyzing pseudogene evolution: implications for silent site evolution in humans and rodents. Mol Biol Evol 19: 110-117. (Pubitemid 34008053)
29. Franzen JL (2005) The implications of the numerical dating of the Messel fossil deposit (Eocene, Germany) for mammalian biochronology. Annales de Paleontologie 91: 329-335.
30. Emry RJ (1970) A North American Oligocene pangolin and other additions to the Pholidota. Bull Amer Mus Nat Hist 142: 455-510.
31. Rose KD, Emry RJ (1993) Relationships of Xenarthra, Pholidota, and fossil "edentates": the morphological evidence. In: Szalay FS, Novacek MJ, McKenna MC, eds. Mammal phylogeny: Placentals. New York: Springer- Verlag. pp 81-102.
32. Simpson GG (1931) Metacheiromys and the Edentata. Bull Amer Mus Nat Hist 59: 295-381.
33. Patterson B, Segall W, Turnbull W, Gaudin T (1992) The ear region in xenarthrans ( = Edentata: Mammalia). Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana Geol new series 24: 1-79.
34. Matthew WD (1918) A revision of the lower Eocene Wasatch and Wind River faunas. Part V. Insectivora (continued), Glires, Edentata. Bull Amer Mus Nat Hist 38: 565-657.
35. Patterson B (1978) Pholidota and Tubulidentata. In: Maglio VJ, Cook HBS, eds. Evolution of African mammals. Cambridge: Harvard Univ Press. pp 268-278.
36. Rose KD (1978) A new Paleocene epoicotheriid (Mammalia), with comments on the Palaeanodonta. J Paleontol 52: 658-674.
37. Rose KD, Emry RJ, Gaudin TJ, Storch G (2005) Xenarthra and Pholidota. In: Rose KD, Archibald JD, eds. The rise of placental mammals. Baltimore: The Johns Hopkins University Press. pp 106-126.
38. Secord R, Gingerich PD, Bloch JI (2002) Mylanodon rosei, a new metacheiromyid (Mammalia, Palaeanodonta) from the late Tiffanian (late Paleocene) of northwestern Wyoming. Contrib Mus Paleontol Univ Michigan 30: 385-399.
39. Gheerbrant E, Rose KD, Godinot M (2005) First palaeanodont (?pholidotan) mammal from the Eocene of Europe. Acta Palaeontol Polon 50: 209-218. (Pubitemid 40919650)
40. Bianucci G, Landini W (2006) Killer sperm whale: a new basal physeteroid (Mammalia, Cetecea) from the Late Miocene of Italy. Zool J Linn Soc 148: 103-131. (Pubitemid 44337266)
41. Fitzgerald EM (2006) A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc R Soc B 273: 2955-2963.
42. Ishiyama M (1987) Enamel structure in odontocete whales. Scanning Microscopy 1: 1071-1079.
43. Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W (2007) Using genomic data to unravel the root of the placental mammal phylogeny. Gen Res 17: 413-421.
44. Simpson GG (1948) The beginning of the age of mammals in South America. Bull Amer Mus Nat Hist 91: 1-232.
45. Lee MSY, Shine R (1998) Reptilian viviparity and Dollo's law. Evolution 52: 1441-1450.
46. Marshall CR, Raff EC, Raff RA (1994) Dollo's law and the death and resurrection of genes. Proc Natl Acad Sci U S A 91: 12283-12287.
47. Kollar EJ, Fisher C (1980) Tooth induction in chick epithelium: expression of quiescent genes for enamel synthesis. Science 207: 993-995.
48. Sire J-Y, Delgado SC, Girondot M (2008) Hen's teeth with enamel cap: from dream to impossibility. BMC Evol Biol 8: 246.
49. Jackman WR, Stock DW (2006) Transgenic analysis of Dlx regulation in fish tooth development reveals evolutionary retention of enhancer function despite organ loss. Proc Natl Acad Sci U S A 103: 19390-19395.
50. Portz DE, Tyus HM (2004) Fish humps in two Colorado River fishes: a morphological response to cyprinid predation? Environ Biol Fishes 71: 233-245.
51. Stock DW, Jackman WR, Trapani J (2006) Developmental genetic mechanisms of evolutionary tooth loss in cypriniform fishes. Development 133: 3127-3137.
52. Werdelin L (1987) Supernumerary teeth in Lynx lynx and the irreversibility of evolution. J Zool 211: 259-266.
53. Gosline WA (1985) A possible relationship between aspects of dentition and feeding in the centrarchid and anabantoid fishes. Environ Biol Fishes 12: 161-168.
54. Stock DW (2001) The genetic basis of modularity in the development and evolution of the vertebrate dentition. Phil Trans R Soc Lond B 356: 1633-1653.
55. Hart PS, Michalec MD, Seow WK, Hart TC, Wright JT (2003) Identification of the enamelin (g.8344delG) mutation in a new kindred and presentation of a standardized ENAM nomenclature. Arch Oral Biol 48: 589-596.
56. Larkin MA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
57. Rambaut A (1996) Se-Al: Sequence Alignment Editor, 2.0a11. http://evolve. zoo.ox.ac.uk.
58. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818. (Pubitemid 28552116)
59. Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
60. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
61. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
62. Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
63. Gatesy J (2009) Whales and even-toed ungulates (Cetartiodactyla). In: Hedges SB, Kumar S, eds. The timetree of life. Oxford: Oxford Univ Press. pp 511-515.
64. Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Syst Biol 51: 689-702. (Pubitemid 35294802)
65. Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15: 1647-1657.
66. Kishino H, Thorne JL, Bruno WJ (2001) Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol Biol Evol 18: 352-361. (Pubitemid 32225084)
67. Springer MS, Murphy WJ, Eizirik E, O'Brien SJ (2003) Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc Natl Acad Sci U S A 100: 1056-1061. (Pubitemid 36183954)
68. Waddell PJ, Kishino H, Ota R (2001) A phylogenetic foundation for comparative mammalian genomics. Genome Inform 12: 141-154.
69. McGowen MR, Spaulding M, Gatesy J (2009) Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol Phylogenet Evol. In press.
70. Chamary JV, Parmley JL, Hurst LD (2006) Hearing silence: non-neutral evolution at synonymous sites in mammals. Nature Genet 7: 98-108.
71. Li W-H, Gojobori T, Nei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292: 237-239.
72. Saitou N, Ueda S (1994) Evolutionary rates of insertion and deletion in noncoding nucleotide sequences of Primates. Mol Biol Evol 11: 504-512. (Pubitemid 24137164)
73. Springer MS, Burk A, Kavanagh JR, Waddell VG, Stanhope MJ (1997) The interphotoreceptor retinoid binding protein gene in therian mammals: Implications for higher level relationships and evidence for loss of function in the marsupial mole. Proc Natl Acad Sci U S A 94: 13754-13759. (Pubitemid 28009656)
74. Bollback JP (2006) SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinf 7: 88.
75. Shockey BJ, Flynn JJ (2007) Morphological diversity in the postcranial skeleton of Casamayoran (?Middle to Late Eocene) Notoungulata and foot posture in notoungulates. Amer Mus Novitat 3601: 1-28.
76. Croft D, Flynn JF, Wyss AR (2008) The Tinguiririca fauna of Chile and the early stages of "modernization" of South American mammal faunas. Arquivos do Museu Nacional, Rio de Janeiro 66: 191-211.