Big and slow: Phylogenetic estimates of molecular evolution in Baleen whales (Suborder Mysticeti)

Molecular Biology and Evolution

Volumn 26, Issue 11, 2009, Pages 2427-2440

  Jackson, J A ^a   Baker, C S ^a,b   Vant, M ^b   Steel, D J ^a   Medrano Gonzalez L ^c   Palumbi, S R ^d  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Cetacean; Genomic; Mitochondrial; Mutation rate; Whale

Indexed keywords

CELL NUCLEUS DNA; CYTOCHROME B; MITOCHONDRIAL DNA;

ANIMAL EXPERIMENT; ARTICLE; BALAENOPTERA; BALEEN WHALE; BODY SIZE; CALIBRATION; CODON; CONTROLLED STUDY; FOSSIL ANIMAL; GENE FREQUENCY; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; HAPLOTYPE; HUMPBACK WHALE; INTRON; MAMMAL; MITOCHONDRIAL GENOME; MITOGENESIS; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROMOTER REGION; SPECIES DIFFERENCE; TAXON; UNINDEXED SEQUENCE; WHALE; ANIMAL; CLASSIFICATION; GENETICS; HUMAN; TIME;

ANIMALIA; BALAENIDAE; BALAENOPTERIDAE; CETACEA; MAMMALIA; MEGAPTERA; MYSTICETI;

ANIMALS; EVOLUTION, MOLECULAR; HUMANS; PHYLOGENY; TIME FACTORS; WHALES;

EID: 73349099032     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp169     Document Type: Article

References (95)

1. Alter SE, Rynes E, Palumbi SR. 2007. DNA evidence for historic population size and past ecosystem impacts of gray whales. Proc Natl Acad Sci USA. 104:15162-15167.
2. Árnason A, Gullberg A, Widegren B. 1991. The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J Mol Evol. 33:556-568.
3. Árnason A, Gullberg A, Widegren B. 1993. Cetacean mitochon-drial DNA control region: sequences of all extant baleen whales and two sperm whale species. Mol Biol Evol. 10:960-970.
4. Ärnason U. 1972. The role of chromosomal rearrangements in mammalian speciation with special reference to Cetacea and Pinnipeda. Hereditas. 70:113-118.
5. Ärnason U. 1974. Comparative chromosome studies in Cetacea. Hereditas. 77:1-36.
6. Ärnason U, Grétarsdóttir S, Widegren B. 1992. Mysticete (Baleen whale) relationships based on the sequence of the common cetacean DNA satellite. Mol Biol Evol. 9:1018-1028.
7. Á rnason Ú, Gullberg A, Grétarsdóttir S, Ursing B, Janke A. 2000. The mitochondrial genome of the sperm whale and a new molecular reference for estimating Eutherian divergence dates. J Mol Evol. 50:569-578.
8. Árnason U, Gullberg A, Janke A. 2004. Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene. 333:27-34.
9. Baker CS, Lento GM, Cipriano F, Palumbi SR. 2000. Predicted decline of protected whales based on molecular genetic monitoring of Japanese and Korean markets. Proc Roy Soc Lond Ser B Biol Sci. 267:1191-1199.
10. Baker CS, Medrano-González L. 2002. Worldwide distribution and diversity of humpback whale mitochondrial DNA lineages. In: Pfeiffer CJ, editor. Molecular and cell biology of marine mammals. Malabar (FL): Krieger Publishing Company. p. 84-99.
11. Baker CS, Medrano-Gonzalez L, Calambokidis J, Perry A, Pichler F, Rosenbaum H, Straley JM, Urban-Ramirez J, Yamaguchi M, Von Ziegesar O. 1998. Population structure of nuclear and mitochondrial DNA variation among humpback whales in the North Pacific. Mol Ecol. 7:695-707.
12. Baker CS, Perry A, Bannister JL, et al. (13 co-authors). 1993. Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc Natl Acad Sci USA. 90:8239-8243.
13. Baker CS, Slade RW, Bannister JL, Abernethy RB, Weinrich MT, Lien J, Urban J, Corkeron P, Calambokidis J, Vasquez O. 1994. Hierarchical structure of mitochondrial DNA gene flow among humpback whales Megaptera novaeangliae, worldwide. Mol Ecol. 3:313-327.
14. Barja G, Herrero A. 2000. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J. 14:312-318.
15. Berubé M, Aguilar A. 1998. A new hybrid between a blue whale, Balaenoptera musculus, and a fin whales, B-physalus: frequency and implications of hybridization. Mar Mammal Sci. 14:82-98.
16. Bromham L, Penny D, Rambaut A, Hendy MD. 2000. The power of relative rates tests depends on the data. J Mol Evol. 50:296-301.
17. Bromham L, Rambaut A, Harvey PH. 1996. Determinants of rate variation in mammalian DNA sequence evolution. J Mol Evol. 43:610-621.
18. Bulmer M, Wolfe KH, Sharp PM. 1991. Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci USA. 88:5974-5978.
19. Caballero S, Jackson JA, Mignucci-Giannoni AA, Barrios-Garrido H, Beltran-Pedreros S, Montiel-Villalobos MA, Robertson KM, Baker CS. 2008. Molecular systematics of South American dolphins Sotalia: sister taxa determination and phylogenetic relationships, with insights into a multi-locus phylogeny of the Delphinidae. Mol Phylogenet Evol. 46:252-268.
20. Carraher CJF. 2004. Comparative mitogenomics of the Southern hemisphere dolphin genus Cephalorhynchus. Auckland (New Zealand): School of Biological Sciences, University of Auckland. p. 161.
21. Cooper A, Fortey R. 1998. Evolutionary explosions and the phylogenetic fuse. Trends Ecol Evol. 13:151-156.
22. Croteau DL, Bohr VA. 1997. Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J Biol Chem. 272:25409-25412.
23. Croteau DL, Stierum RH, Bohr VA. 1999. Mitochondrial DNA repair pathways. Mut Res. 434:137-148.
24. Deméré TA, Berta A, McGowen MR. 2005. The taxonomic and evolutionary history of fossil and modern balaenopterid mysticetes. J Mamm Evol. 12:99-143.
25. 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.
26. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylogenies and dating with confidence. PLoS Biol 4:699-710.
27. Drummond AJ, Rambaut A. 2007. BEAST v1.4.7. Oxford: University of Oxford.
28. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian c inference of past population dynamics from molecular sequences. Mol Biol Evol. 22:1185-1192.
29. Emerson BC. 2007. Alarm bells for the molecular clock? No support for Ho et al.'s model of time-dependent molecular rate estimates. Syst Biol. 56:337-345.
30. Endicott P, Ho SYW. 2008. A Bayesian evaluation of human mitochondrial substitution rates. Am J Hum Genet. 82: 895-902.
31. Engel MH, Fagundes NJR, Rosenbaum HC, Leslie MS, Ott PH, Schmitt R, Secchi E, Dalla Rosa L, Bonatto SL. 2008. Mitochondrial DNA diversity of the Southwestern Atlantic humpback whale (Megaptera novaeangliae) breeding area off Brazil, and the potential connections to Antarctic feeding areas. Conserv Genet. 9:1253-1262.
32. Ewing B, Green P. 1998. Basecalling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186-194. (Pubitemid 28177230)
33. Ewing B, Hillier L, Wendl M, Green P. 1998. Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185. (Pubitemid 28177229)
34. Farris JS. 1989. The retention index and homoplasy excess. Syst Zool. 38:406-407.
35. Fenner JN. 2005. Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am J Phys Anthropol. 128:415-423.
36. Fordyce RE. 1989. Origins and evolution of Antarctic marine mammals. Geol Soc Lond Spec Publ. 47:269-281.
37. Fordyce RE. 2002. Oligocene origins of skim-feeding right whales: a small archaid balaenid from New Zealand. J Vertebr Paleontol. 22:54a.
38. Fordyce RE, Barnes LG. 1994. The evolutionary history of whales and dolphins. Annu Rev Earth Planet Sci. 22:419-455.
39. Friesen VL, Congdon BC, Walsh HE, Birt TP. 1997. Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Mol Ecol. 6:1047-1058.
40. Gillooly JF, Allen AP, West GB, Brown JH. 2005. The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc Natl Acad Sci USA. 102:140-145.
41. Gradstein FM, Ogg JG. 2004. Geologic Time Scale 2004-why, how, and where next!. Lethaia. 37:175-181.
42. Hardison RC, Roskin KM, Yang S, et al. (17 co-authors). 2003. Covariation in frequencies of substitution, deletion, transposition, and recombination during Eutherian evolution. Genome Res. 13:13-26.
43. Harman D. 1957. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 2:298-300.
44. Hasegawa M, Kishino K, Yano T. 1985. Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 22:160-174.
45. Hoelzel AR, Hancock JM, Dover GA. 1991. Evolution of the cetacean mitochondrial D-loop region. Mol Biol Evol. 8:475-493.
46. Hurvich CM, Tsai C-L. 1989. Regression and time series model selection in small samples. Biometrika. 76:297-307.
47. Jablonski D, Bottjer DJ. 1990. The origin and diversification of major groups: environmental patterns and macroevolutionary lags. Pp. 17-58 In: Taylor PD, Larwood GP, editor. Major evolutionary radiations. Clarendon Press: Oxford.
48. Kimura T, Ozawa T. 2002. Rates of mitochondrial DNA evolution are slower in mysticete relative to Odontocete Cetaceans. In: Pfeiffer CJ, editor. Molecular and cell biology of marine mammals. Malabar (FL): Krieger Publishing Company. p. 111-117.
49. Kumar S, Subramanian S. 2002. Mutation rates in mammalian genomes. Proc Natl Acad Sci, USA. 99:803-808.
50. Lambertsen RH. 1987. A biopsy system for large whales and its use for cytogenetics. J Mamm. 68:443-445.
51. Lasken RS, Egholm M. 2003. Whole genome amplification: abundant supplies of DNA from precious samples or clinical specimens. Trends Biotechnol. 21:531-535.
52. Li W-H. 1997. Molecular evolution. Sunderland (MA): Sinauer Associates.
53. Li WH, Tanimura M, Sharp PM. 1987. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol. 25:330-342.
54. Li WH, Yi S, Makova K. 2002. Male-driven evolution. Curr Opin Genet Dev. 12:650-656.
55. Liu P, Qian L, Sung JS, de Souza-Pinto NC, Zheng L, Bogenhagen DF, Bohr VA, Wilson DM, Shen B, Dernple B. 2008. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol Cell Biol. 28:4975-4987.
56. Lyons LA, Laughlin TF, Copeland NG, Jenkins NA, Womack JE, O'Brien SJ. 1997. Comparative anchor tagged sequences (CATS) for integrative mapping of mammalian genomes. Nat Genet. 15:47-56.
57. Maddison DR, Maddison WP. 2005. MacClade 4. Sunderland (MA): Sinauer Associates, Inc.
58. Makalowski W, Boguski M. 1998. Evolutionary parameters of the transcribed mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc Natl Acad Sci USA. 95:9407-9412.
59. Martin AP, Palumbi S. 1993. Body size, metabolic rate, generation time and the molecular clock. Proc Natl Acad Sci USA. 90:4087-4091.
60. Matsumura S, Forster P. 2008. Generation time and effective population size in Polar Eskimos. Proc Roy Soc Lond Ser B Biol Sci. 275:1501-1508.
61. McVean GT, Hurst LD. 1997. Evidence for a selectively favourable reduction in the mutation rate of the X chromosome. Nature. 386:388-392.
62. Milinkovitch MC. 1995. Molecular phylogeny of cetaceans prompts revision of morphological transformations. Trends Ecol Evol. 10:328-334.
63. Milinkovitch MC, Bérubé M, Palsbøll PJ. 1998. Cetaceans are highly specialized artiodactyls. In: Thewissen JGM, editor. The emergence of whales: evolutionary patterns in the origin of Cetacea. New York: Plenum.
64. Mitchell ED. 1989. A new cetacean from the Late Eocene La Meseta formation, Seymour Island, Antarctic Peninsula. Can J Fish Aquat Sci. 46:2219-2235.
65. Nabholz B, Glémin S, Galtier N. 2008. Strong variations of mitochondrial mutation rate across mammals\the longevity hypothesis. Mol Biol Evol. 25:120-130.
66. Nachman MW, Crowell SL. 2000. Estimate of the mutation rate per nucleotide in humans. Genetics. 156:297-304.
67. Nikaido M, Hamilton H, Makino H, Sasaki T, Takahashi K, Goto M, Kanda N, Pastene L, Okada N. 2006. Baleen whale phylogeny and a past extensive radiation event revealed by SINE insertion analysis. Mol Biol Evol. 23: 866-873.
68. Nikaido M, Matsuno F, Hamilton H, Brownell RL Jr., Cao Y, Ding W, Zuoyan Z, Shedlock AM, Fordyce RE, Hasegawa M, Okada N. 2001. Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA. 98:7384-7389.
69. Nikolaev SI, Montoya-Burgos JI, Popadin K, Parand L, Margulles EH, National Institutes of Health Intramural Sequencing Center Comparative Sequencing Program, Antonarakis SE. 2007. Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements. Proc Natl Acad Sci USA. 104:20443-20448.
70. Nishida S, Goto M, Pastene L, Kanda N, Koike H. 2007. Phylogenetic relationships among cetaceans revealed by Y-chromosome sequences. Zool Sci. 24:723-732.
71. Olavarría C, Baker CS, Garrigue C, et al. (19 co-authors). 2007. Population structure of South Pacific humpback whales and the origin of the eastern Polynesian breeding grounds. Mar Ecol Prog Ser. 330:257-268.
72. Palumbi SR. 1995. Nucleic acids II: the polymerase chain reaction. In: Hillis D, Moritz C, Mable BK, editors. Molecular systematics. Sunderland (MA): Sinauer Associates, Inc.
73. Palumbi SR, Baker CS. 1994. Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales. Mol Biol Evol. 11:426-435.
74. Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics. 14:817-818.
75. Rambaut A, Drummond AJ. 2007. Tracer: MCMC trace analysis tool v1.4. Oxford: University of Oxford.
76. Rohland N, Malaspinas A, Pollack JL, Slatkin M, Matheus P, Hofreiter M. 2007. Proboscidean mitogenomics: chronology and mode of elephant evolution using Mastodon as outgroup. PLoS Biol. 5:1663-1671.
77. Rooney AP, Honeycutt RL, Derr JN. 2001. Historical population size change of bowhead whales inferred from DNA sequence polymorphism data. Evolution. 55:1678-1685.
78. Rosenbaum HC, Pomilla CC, Leslie MC, et al. (21 co-authors). PLoS ONE, in press. Mitochondrial DNA diversity and population structure of humpback whales from their breeding areas in the south Atlantic and Indian Oceans (breeding regions A, B, C and X).
79. Rosenbaum HC, Weinrich MT, Stoleson SA, Gibbs JP, Baker CS, DeSalle R. 2002. The effect of differential reproductive success on population genetic structure: correlations of life history with matrilines in humpback whales of the Gulf of Maine. J Hered. 93:389-399.
80. Rychel AL, Reeder TW, Berta A. 2004. Phylogeny of mysticete whales based on mitochondrial and nuclear data. Mol Phylogenet Evol. 32:892-901.
81. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. 1988. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 239:487-491.
82. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory.
83. Sasaki T, Nikaido M, Hamilton H, et al. (10 co-authors). 2005. Mitochondrial phylogenetics and evolution of mysticete whales. Syst Biol. 54:77-90.
84. Scheet P, Stephens M. 2006. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Amer J Hum Genet. 78:629-644.
85. Schlötterer C, Amos B, Tautz D. 1991. Conservation of polymorphic simple sequence loci in cetacean species. Nature. 354:63-65.
86. Spilliaert R, Vikingsson G, Á rnason Ú, Palsdottir A, Sigurjonsson J, Á rnason A. 1991. Species hybridization between a female blue whale (Balaenoptera musculus) and a male fin whale (B. physalus): Molecular and morphological documentation. J Hered. 82:269-274.
87. Swofford DL. 2002. PAUP: phylogenetic analysis using parsimony, 4.0b.10. Sunderland (MA): Sinauer Associates.
88. Takezaki N, Rzhetsky A, Nei M. 1995. Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol. 12:823-833.
89. Taylor BL, Chivers SJ, Larese J, Perrin WF. 2007. Generation length and percent mature estimates for IUCN assessments of cetaceans. La Jolla (CA): National Marine Fisheries Service, Southwest Fisheries Science Center. p. 1-24.
90. Thorne JL, Kishino H, Painter IS. 1998. Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol. 15:1647-1657.
91. Uhen MD. 1998. Middle to late Eocene Basilosaurines and Dorudontines. In: Thewissen JGM, editor. The emergence of whales. New York: Plenum Press. p. 29-61.
92. Uhen MD. 1999. New species of protocetid Archaeocete whale, Eocetus wardii (Mammalia: Cetacea) from the middle Eocene of North Carolina. J Paleontol. 73:512-528.
93. Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC. 1991. African populations and the evolution of human mitochondrial DNA. Science. 253:1503-1507.
94. West GB, Brown JH, Enquist BJ. 1997. A general model for the origin of allometric scaling laws in biology. Science. 276:122-126.
95. Yang Z, Rannala B. 1997. Bayesian phylogenetic inference using DNA sequences: a Markov chain Monte Carlo method. Mol Biol Evol. 14:717-724.