Evidence of positive selection in mitochondrial complexes I and V of the African elephant

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Finch, Tabitha M ^a   Zhao, Nan ^b   Korkin, Dmitry ^c   Frederick, Katy H ^a   Eggert, Lori S ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL COMPLEX V; MITOCHONDRIAL DNA; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN;

ANIMAL GENETICS; ARTICLE; BIOCHEMISTRY; DNA SEQUENCE; ELEPHANT; ENZYME STRUCTURE; GENETIC SELECTION; HABITUAL ADAPTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SPECIES IDENTIFICATION; ADAPTATION; ANIMAL; GENETICS; MOLECULAR EVOLUTION; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ELECTRON TRANSPORT COMPLEX I; ELEPHANTS; EVOLUTION, MOLECULAR; MITOCHONDRIAL PROTEINS; SELECTION, GENETIC;

EID: 84898925931     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092587     Document Type: Article

References (69)

1. Smith NGC, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415: 1022-1024. (Pubitemid 34193448)
2. Dalziel AC, Rogers SM, Schulte PM (2009) Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Molecular Ecology 18: 4997-5017.
3. Krause J, Dear P, Pollack J, Slatkin M, Spriggs H, et al. (2006) Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature 439: 724-727. (Pubitemid 43237618)
4. Rohland N, Malaspinas A, Pollack J, Slatkin M, Matheus P, et al. (2007) Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biology 5: e207.
5. Brandt AL, Ishida Y, Georgiadis NJ, Roca AL (2012) Forest elephant mitochondrial genomes reveal that elephantid diversification in Africa tracked climate transitions. Molecular Ecology 21: 1175-1189.
6. Roca A, Georgiadis N, Pecon-Slattery J, O'Brien S (2001) Genetic evidence for two species of elephant in Africa. Science 293: 1473-1477. (Pubitemid 32801548)
7. White LJT, Tutin CEG, Fernandez M (1993) Group composition and diet of forest elephants, Loxodonta africana cyclotis Matschie 1900, in the Lopé Reserve, Gabon. African Journal of Ecology 31: 181-199. (Pubitemid 24416865)
8. Lister AM (2013) The role of behaviour in adaptive morphological evolution of African proboscideans. Nature advance online publication.
9. Codron J, Codron D, Lee-Thorp J, Sponheimer M, Kirkman K, et al. (2011) Landscape-scale feeding patterns of African elephant inferred from carbon isotope analysis of feces. Oecologia 165: 89-99.
10. Owen-Smith RN (1988) Megaherbivores: Cambridge University Press.
11. Sikes SK (1971) The Natural History of the African Elephant. London: Weidenfeld and Nicolson.
12. Rand DM, Kann LM (1998) Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica 102-103: 393-407. (Pubitemid 28371732)
13. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303: 223-226. (Pubitemid 38057570)
14. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570-572.
15. Wallace DC (1992) Diseases of the mitochondrial DNA. Annual Review of Biochemistry 61: 1175-1212.
16. Rankinen T, Bray MS, Hagberg JM, Pérusse L, Roth SM, et al. (2006) The human gene map for performance and health-related fitness phenotypes: The 2005 update. Medicine and Science in Sports and Exercise 38: 1863-1888. (Pubitemid 44707790)
17. Grossman LI, Schmidt TR, Wildman DE, Goodman M (2001) Molecular evolution of aerobic energy metabolism in primates. Molecular Phylogenetics and Evolution 18: 26-36. (Pubitemid 32113873)
18. Goodman M, Sterner KN, Islam M, Uddin M, Sherwood CC, et al. (2009) Phylogenomic analyses reveal convergent patterns of adaptive evolution in elephant and human ancestries. Proceedings of the National Academy of Sciences 106: 20824-20829.
19. da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics 9.
20. Grossman LI, Wildman DE, Schmidt TR, Goodman M (2004) Accelerated evolution of the electron transport chain in anthropoid primates. TRENDS in Genetics 20: 578-585. (Pubitemid 39314566)
21. Garvin MR, Bielawski JP, Gharrett AJ (2011) Positive Darwinian Selection in the Piston That Powers Proton Pumps in Complex I of the Mitochondria of Pacific Salmon. PLoS ONE 6: e24127.
22. Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621-628.
23. Sánchez R, Šali A (2000) Comparative protein structure modeling: introduction and practical examples with modeller. Methods in Molecular Biology 143: 97-129.
24. Murata Y, Yonezawa T, Kihara I, Kashiwamura T, Sugihara Y, et al. (2009) Chronology of the extant African elephant species and case study of the species identification of the small African elephant with the molecular phylogenetic method. Gene 441: 176-186.
25. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Research 28: 235-242. (Pubitemid 30047768)
26. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494: 443-448.
27. Efremov RG, Sazanov LA (2011) Structure of the membrane domain of respiratory complex I. Nature 476: 414-420.
28. Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J, et al. (2006) Bovine Complex I Is a Complex of 45 Different Subunits. Journal of Biological Chemistry 281: 32724-32727. (Pubitemid 46036828)
29. Balsa E, Marco R, Perales-Clemente E, Szklarczyk R, Calvo E, et al. (2012) NDUFA4 Is a Subunit of Complex IV of the Mammalian Electron Transport Chain. Cell Metabolism 16: 378-386.
30. Walker JE (1992) The NADH: ubiquinone oxidoreductase (complex I) of respiratory chains. Quarterly Review of Biophysics 25: 253-324.
31. Radermacher M, Ruiz T, Clason T, Benjamin S, Brandt U, et al. (2006) The three-dimensional structure of complex I from Yarrowia lipolytica: A highly dynamic enzyme. Journal of Structural Biology 154: 269-279. (Pubitemid 43737264)
32. Miller S, Janin J, Lesk AM, Chothia C (1987) Interior and surface of monomeric proteins. Journal of molecular biology 196: 641-656.
33. Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465: 441-445.
34. Taylor WR (1986) The classification of amino acid conservation. Journal of Theoretical Biology 119: 205-218.
35. Arsenieva D, Symersky J, Wang Y, Pagadala V, Mueller DM (2010) Crystal Structures of Mutant Forms of the Yeast F1 ATPase Reveal Two Modes of Uncoupling. Journal of Biological Chemistry 285: 36561-36569.
36. Weber J, Senior AE (1997) Catalytic mechanism of F1-ATPase. Biochimica et Biophysica Acta 1319: 19-58.
37. Xu S, Luosang J, Hua S, He J, Ciren A, et al. (2007) High Altitude Adaptation and Phylogenetic Analysis of Tibetan Horse Based on the Mitochondrial Genome. Journal of Genetics and Genomics 34: 720-729. (Pubitemid 47247621)
38. Ning T, Xiao H, Li J, Hua S, Zhang YP (2010) Adaptive evolution of the mitochondrial ND6 gene in the domestic horse. Genetics and Molecular Research 9: 144-150.
39. Eggert LS, Rasner CA, Woodruff DS (2002) The evolution and phylogeography of the African elephant inferred from mitochondrial DNA sequence and nuclear microsatellite markers. Proceedings of the Royal Society B: Biological Sciences 269: 1993-2006. (Pubitemid 35177009)
40. Johnson MB, Clifford SL, Goossens B, Nyakaana S, Curran B, et al. (2007) Complex phylogeographic history of central African forest elephants and its implications for taxonomy. BMC Evolutionary Biology 7.
41. Foote AD, Morin PA, Durban JW, Pitman RL, Wade P, et al. (2010) Positive selection on the killer whale mitogenome. Biology Letters.
42. Ballard JWO, Melvin RG, Katewa SD, Maas K (2007) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution 61: 1735-1747. (Pubitemid 47013468)
43. Peters RH (1986) The ecological implications of body size: Cambridge University Press.
44. Morgan BJ, Lee PC (2003) Forest elephant (Loxodonta africana cyclotis) stature in the Réserve de Faune du Petit Loango, Gabon. Journal of Zoology 259: 337-344. (Pubitemid 36434969)
45. Piccoli C, Ripoli M, Scrima R, Stanziale P, Di Ianni M, et al. (2008) MtDNA mutation associated with mitochondrial dysfunction in megakaryoblastic leukaemic cells. Leukemia 22: 1938-1941.
46. McNab BK (1983) Energetics, body size, and the limits to endothermy. Journal of Zoology 199: 1-29.
47. Williams TM (1990) Heat transfer in elephants: thermal partitioning based on skin temperature profiles. Journal of Zoology 222: 235-245.
48. Mishmar D, Ruiz-Pesini E, Golik P, Macaulay V, Clark AG, et al. (2003) Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences 100: 171-176. (Pubitemid 36078047)
49. Deribe YL, Pawson T, Dikic I (2010) Post-translational modifications in signal integration. Nature Structural & Molecular Biology 17: 666-672.
50. Schuttler SG (2012) The secret lives of African forest elephants: using genetics, networks, and telemetry to understand sociality: University of Missouri-Columbia.
51. Roca A, O'Brien S (2005) Genomic inferences from Afrotheria and the evolution of elephants. Curr Opin Genet Dev 15: 652-659. (Pubitemid 41534656)
52. Amos W, Whitehead H, Ferrari MJ, Glockner-Ferrari DA, Payne R, et al. (1992) Restrictable DNA from sloughed cetacean skin; its potential for use in population analysis. Marine Mammal Science 8: 275-283.
53. Eggert LS, Maldonado JE, Fleischer RC (2005) Nucleic acid isolation from ecological samples-animal scat and other associated materials. Methods in Enzymology 395: 73-82.
54. Archie EA, Moss CJ, Alberts SC (2006) The ties that bind: Genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proceedings of the Royal Society B: Biological Sciences 273: 513-522. (Pubitemid 46768054)
55. Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology & Evolution 16: 314-321. (Pubitemid 32706648)
56. Greenwood AD, Pääbo S (1999) Nuclear insertion sequences of mitochondrial DNA predominate in hair but not in blood of elephants. Molecular Ecology 8: 133-137. (Pubitemid 29032683)
57. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, et al. (2013) GenBank. Nucleic Acids Research 41: D36-D42.
58. Tao N, Bruno WJ, Abfalterer W, Moret BM, Leitner T, et al. (2005) FINDMODEL: a tool to select the best-fit model of nucleotide substitution: University of New Mexico.
59. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science 294: 2310-2314. (Pubitemid 33140548)
60. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
61. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307-321.
62. Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Molecular Biology and Evolution 15: 568-573.
63. Woolley S, Johnson J, Smith MJ, Crandall KA, McClellan DA (2003) TreeSAAP: Selection on amino acid properties using phylogenetic trees. Bioinformatics 19: 671-672. (Pubitemid 36417070)
64. Sali A, Blundell T (1994) Comparative protein modelling by satisfaction of spatial restraints. Protein Structure by Distance Analysis 64: C86.
65. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-A visualization system for exploratory research and analysis. Journal of Computational Chemistry 25: 1605-1612.
66. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, et al. (2005) The FoldX web server: an online force field. Nucleic Acids Research 33: W382-W388. (Pubitemid 44529948)
67. Zhang Y, Skolnick J (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Research 33: 2302-2309. (Pubitemid 41439897)
68. Zhang Y, Skolnick J (2004) Scoring function for automated assessment of protein structure template quality. Proteins: Structure, Function, and Bioinformatics 57: 702-710. (Pubitemid 39626992)
69. Hubbard SJ, Thornton JM (1993) Naccess. Computer Program, Department of Biochemistry and Molecular Biology, University College London 2.