Relaxed clocks and inferences of heterogeneous patterns of nucleotide substitution and divergence time estimates across whales and dolphins (Mammalia: Cetacea)

Molecular Biology and Evolution

Volumn 29, Issue 2, 2012, Pages 721-736

  Dornburg, Alex ^a   Brandley, Matthew C ^a,c   McGowen, Michael R ^b,d   Near, Thomas J ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

divergence times; molecular clock; Mysticeti; Odontoceti; rate heterogeneity; uncorrelated relaxed clock

Indexed keywords

ACCURACY; AGE DETERMINATION; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; DOLPHIN; GENETIC HETEROGENEITY; GENETIC VARIABILITY; MITOCHONDRIAL GENE; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PHYLOGENY; SIMULATION; WHALE;

ANIMALS; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; DOLPHINS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME; GENOME, MITOCHONDRIAL; MITOCHONDRIA; MUTATION; NUCLEOTIDES; PHYLOGENY; TIME FACTORS; WHALES;

CETACEA; MAMMALIA; MYSTICETI; ODONTOCETI;

EID: 84855870606     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr228     Document Type: Article

References (128)

1. Abdo Z, Minin VN, Joyce P, Sullivan J. 2005. Accounting for uncertainty in the tree topology has little effect on the decisiontheoretic approach to model selection in phylogeny estimation. Mol Biol Evol. 22:691-703. (Pubitemid 40299518)
2. Akaike H. 1973. Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F, editors. Second annual symposium on information theory. Budapest (Hungary): Akademi Kiado. p. 267-281.
3. Alter SE, Palumbi SR. 2009. Comparing evolutionary patterns and variability in the mitochondrial control region and cytochrome b in three species of baleen whales. J Mol Evol. 68:97-111.
4. Aris-Brosou S, Yang Z. 2002. Effects of models of rate evolution on estimation of divergence dates with special reference to the metazoan 18S ribosomal RNA phylogeny. Syst Biol. 51:703-714. (Pubitemid 35294803)
5. Baer CF, Miyamoto MM, Denver DR. 2007. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat Rev Genet. 8:619-631. (Pubitemid 47077282)
6. Barnes LG, Domning DP, Ray CE. 1985. Status of studies on fossil marine mammals. Mar. Mamm Sci. 1:15-53. (Pubitemid 16299662)
7. Bininda-Emonds ORP. 2007. Fast genes and slow clades: comparative rates of molecular evolution in mammals. Evol Bioinform. 3:59-85.
8. Bisconti M. 2007. A new basal balaenopterid whale from the Pliocene of Northern Italy. Palaeontology 50:1103-1122. (Pubitemid 47433973)
9. Bouetel V, de Muizon C. 2006. The anatomy and relationships of Piscobalaena nana (Cetacea, Mysticeti), a Cetotheriidae s.s.from the early Pliocene of Peru. Geodiversitas 28:319-395. (Pubitemid 44211476)
10. Brandley MC, Wang Y, Guo X, Nieto Montes de Oca A, Ferio Ortís M, Hikida T, Ota H. 2011. Accommodating locus-specific heterogeneity in molecular dating methods: an example using inter-continental dispersal of Plestiodon (Eumeces) lizards. Syst Biol. 60:3-15.
11. Britten RJ. 1986. Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393-1398. (Pubitemid 16046651)
12. Bromham L. 2002. Molecular clocks in reptiles: life history influences rate of molecular evolution. Mol Biol Evol. 19:302-309. (Pubitemid 34187641)
13. Bromham L. 2009. Why do species vary in their rate of molecular evolution? Biol Lett. 5:401-404.
14. Bromham L, Leys R. 2005. Sociality, population size and rate of molecular evolution. Mol Biol Evol. 22:1393-1402. (Pubitemid 40740250)
15. Bromham L, Penny D. 2003. The modern molecular clock. Nat Rev Gen. 4:216-224. (Pubitemid 36277637)
16. Chatterjee HS, Ho SYW, Barnes I, Goves C. 2009. Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol Biol. 9:259.
17. Dathe F. 1983. Megaptera hubachi n. sp, ein fossiler Bartenwal aus marinen Sandsteinschichten des tieferen Pliozäns Chiles. Z Geol Wiss (Berl). 11:813-848.
18. de Muizon C. 1988. Les vertébrés fossiles de la Formation Pisco (Pérou). III. Les odontocètes du Miocène. Editions Recherche sur les Civilisations Mémoire. Vol. 78. Paris: ERC. p. 1-244.
19. Deméré TA, Berta A, McGowen MR. 2005. The taxonomic and evolutionary history of fossil and modern balaenopterid mysticetes. J Mamm Evol. 12:99-143. (Pubitemid 41779897)
20. 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.
21. Dornburg A, Beaulieu JM, Oliver JC, Near TJ. 2011. Integrating fossil preservation biases in the selection of calibrations for molecular divergence time estimation. Syst Biol. 60:519-527.
22. Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998. Rates of spontaneous mutation. Genetics 148:1667.
23. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
24. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214.
25. Drummond AJ, Suchard MA. 2010. Bayesian random local clocks, or one rate to rule them all. BMC Biol. 8:114.
26. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
27. 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.
28. Fajardo-Mellor L, Berta A, Brownell RL Jr, Boy CC, Goodall RNP. 2006. The phylogenetic relationships and biogeography of true porpoises (Mammalia: Phocoenidae) based on morphological data. Mar. Mamm Sci. 22:910-932. (Pubitemid 44434880)
29. Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 17:368-376. (Pubitemid 11016207)
30. Fitzgerald EMG. 2006. A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc R Soc B. 273:2955-2963. (Pubitemid 46622425)
31. Fitzgerald EMG. 2010. The morphology and systematics of Mammalodon colliveri (Cetacea:Mysticeti), a toothed mysticete from the Oligocene of Australia. Zool J Linn Soc. 158:367-476.
32. Fordyce RE. 2002. Oligocene origins of skim-feeding right whales: a small archaic balaenid from New Zealand. J Vertebr Paleontol. 22 (Suppl 3):54A.
33. Fordyce RE. 2003. Cetacea evolution and Eocene-Oligocene oceans revisited. In: Prothero DR, Ivany LC, Nesbitt E, editors. From greenhouse to icehouse. The marine Eocene-Oligocene transition. New York: Columbia University Press. p. 154-170.
34. Fordyce RE, Barnes LG. 1994. The evolutionary history of whales and dolphins. Island Arc. 3:373-391.
35. Galtier N, Jobson RW, Nabholz B, Glémin S, Blier PU. 2009. Mitochondrial whims: metabolic rate, longevity, and the rate of molecular evolution. Biol Lett. 5:413-416.
36. Gatesy J. 1997. More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene γ-fibrinogen. Mol Biol Evol. 14:537-543. (Pubitemid 27200484)
37. Gatesy J, Milinkovitch M, Waddell V, Stanhope M. 1999. Stability of cladistic relationships between Cetacea and higher level artiodactyl taxa. Syst Biol. 48:6-20.
38. Geisler JH, Uhen MD. 2003. Morphological support for a close relationship between hippo and whales. J Vertebr Paleontol. 23:991-996.
39. 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 U S A. 102:140-145. (Pubitemid 40094442)
40. Gingerich PD, Russel DE. 1981. Pakicetus inachus, a new archaeocete (Mammalia, Cetacea) from the Early-Middle Eocene Kuldana Formation of Kohat (Pakistan). Contrib Mus Paleontol Univ Mich. 25:235-246.
41. Gingerich PD, Haq MU, Zalmout IS, Khan IH, Malkani MS. 2001. Origin of whales from early artiodactyls: hands and feet of Eocene protocetidae from Pakistan. Science 293:2239-2242. (Pubitemid 32900230)
42. Goldberg A, Wildman DE, Schmidt TR, Huttemann M, Goodman M, Weiss ML, Grossman LI. 2003. Adaptive evolution of cytochrome c oxidase subunit VIII in anthropoidprimates. Proc Natl Acad Sci U S A. 100:5873-5878. (Pubitemid 36576900)
43. Goremykin VV, Hirsch-Ernst KI, Wölfl S, Hellwig FH. 2004. The chloroplast genome of Nymphaea alba: whole-genome analyses and the problem of identifying the most basal angiosperm. Mol Biol Evol. 21:1445-1454. (Pubitemid 38823747)
44. Hamilton H, Caballero S, Collins AG, Brownell RL Jr. 2001. Evolution of river dolphins. Proc R Soc B. 268:549-556. (Pubitemid 32250792)
45. Heled J, Drummond AJ. 2011. Calibrated tree priors for relaxed phylogenetics and divergence time estimation. Syst Biol. Advance Access published August 18, 2011, doi: 10.1093/sysbio/syr087.
46. Hillis DM, Mable BK, Moritz C. 1996. Applications of molecular systematics: the state of the field a look to the future. In: Hillis DM, Moritz C, Mable BK, editors. Molecular systematics. Sunderland (MA): Sinauer Associates.
47. Ho SYW. 2009. An examination of phylogenetic models of substitution rate variation among lineages. Biol Lett. 5:421-424.
48. Ho SYW, Lanfear R. 2010. Improved characterisation of amonglineage rate variation in cetacean mitogenomes using codonpartitioned relaxed clocks. Mitochondrial DNA. 21:138-146.
49. Ho SYW, Phillips MJ. 2009. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol. 58:367-380.
50. Ho SYW, Phillips MJ, Cooper A, Drummond AJ. 2005. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol. 22:1561-1568. (Pubitemid 40800685)
51. Ho SYW, Phillips MJ, Drummond AJ, Cooper A. 2005. Accuracy of rate estimation using relaxed clock models, with a critical focus on the early metazoan radiation. Mol Biol Evol. 22:1355-1363. (Pubitemid 40577774)
52. Hoehna S, Drummond AJ. 2011. Guided tree topology proposals for Bayesian phylogenetic inference. Syst Biol. Advance Access published August 9, 2011, doi:10.1093/sysbio/syr074.
53. Holland SM, Patzkowsky SE. 2002. Stratiographic variation in the timing of first and last occurances. Palaios 17:134-146. (Pubitemid 34573161)
54. Huelsenbeck JP, Larget B, Swofford D. 2000. A compound Poisson process for relaxing the molecular clock. Genetics 154:1879-1892. (Pubitemid 30211265)
55. Inoue J, Donoghue PCJ, Yang Z. 2010. The impact of the representation of fossil calibrations on Bayesian estimation of species divergence times. Syst Biol. 59:74-89.
56. Irwin DM, Árnason U. 1994. Cytochrome b gene of marine mammals: phylogeny and evolution. J Mamm Evol. 2:37-55.
57. Jackson JA, Baker CS, Vant M, Steel DJ, Medrano-González L, Palumbi SR. 2009. Big and slow: phylogenetic estimates of molecular evolution in baleen whales (suborder Mysticeti). Mol Biol Evol. 26:2427-2440.
58. Jiang ZJ, Castoe TA, Austin CC, Burbrink FT, Herron MD, McGuire JA, Parkinson CL, Pollock DD. 2007. Comparative mitochondrial genomics of snakes: extraordinary substitution rate dynamics and functionality of the duplicate control region. BMC Evol Biol. 7:123.
59. Jorba J, Campagnoli R, De L, Kew O. 2008. Calibration of multiple poliovirus molecular clocks covering an extended evolutionary range. J Virol. 82:4429-4440. (Pubitemid 351563679)
60. Kay RF, Fleagle JG, Mitchell TRT, Colbert M, Bown T, Powers DW. 2008. The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina. J Hum Evol. 54:323-382. (Pubitemid 351228709)
61. 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.
62. Lambert O, Bianucci G, Post K. 2009. A new beaked whale (Odontoceti, Ziphiidae) from the middle Miocene of Peru. J Vertebr Paleontol. 29:910-922.
63. Lanfear R, Thomas JA, Welch JJ, Brey T, Bromham L. 2007. Metabolic rate does not calibrate the molecular clock. Proc Natl Acad Sci U S A. 104:15388-15393. (Pubitemid 47502927)
64. Lepage T, Bryant D, Philippe H, Lartillot N. 2007. A general comparison of relaxed molecular clock models. Mol Biol Evol. 24:2669-2680.
65. Li WH. 1997. Molecular evolution, 1st ed. Sunderland (MA): Sinauer Press.
66. Lopez P, Casane D, Philippe H. 2002. Heterotachy, an important process of protein evolution. Mol Biol Evol. 19:1-7. (Pubitemid 34008041)
67. Lopez-Giraldez F, Townsend JP. 2011. PhyDesign: an online application for profiling phylogenetic informativeness. BMC Evol Biol. 11:152.
68. Lu PJ, Yogo M, Marshall CR. 2006. Phanerozoic marine biodiversity dynamics in light of the incompleteness of the fossil record. Proc Natl Acad Sci U S A. 103:2736-2739.
69. Marshall CR. 1990. Confidence intervals on stratigraphic ranges. Paleobiology 16:1-10. (Pubitemid 20416616)
70. Marshall CR. 2008. A simple method for bracketing absolute divergence times on molecular phylogenies using multiple fossil calibrations points. Am Nat. 171:726-742. (Pubitemid 351706502)
71. Martin AP, Palumbi SR. 1993. Body size, metabolic-rate, generation time, and the molecular clock. Proc Natl Acad Sci U S A. 90:4087-4091. (Pubitemid 23134171)
72. Marx FG, Uhen MD. 2010. Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales. Science 327:993-996.
73. McGowen MR, Spaulding M, Gatesy J. 2009. Divergence data estimation and a comprehensive molecular tree of extant cetaceans. Mol Phylogenet Evol. 53:891-906.
74. Mchedlidze GA. 1970. Nekotorye Obshie Cherty Istorii Kitoobraznykh. [Some general characteristics of the evolution of Cetaceans]. Tbilisi (Georgia): Metsniereba Press, Institut Paleobiologii Akademia Nauk, Gruzinskoi SSR.
75. Meredith RW, Gatesy J, Murphy WJ, Ryder OA, Springer MS. 2009. Molecular decay of the tooth gene enamelin (ENAM) mirrors the loss of enamel in the fossil record of placental mammals. PLoS Genet. 5:e1000634.
76. Messenger SL, McGuire JA. 1998. Morphology, molecules, and the phylogenetics of Cetaceans. Syst Biol. 47:90-124. (Pubitemid 128449788)
77. Milinkovitch MC. 1995. Molecular phylogeny of cetaceans prompts revision of morphological transformations. Trends Ecol Evol. 10:328-334.
78. 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.
79. Mooers AO, Harvey PH. 1994. Metabolic rate, generation time and the rate of molecular evolution in birds. Mol Phylogenet Evol. 3:344-350.
80. Montgelard C, Catzefelis FM, Douzery E. 1997. Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. Mol Biol Evol. 14:550-559. (Pubitemid 27200486)
81. Nabholz B, Glemin S, Galtier N. 2008. Strong variation of mitochondrial mutation rate across mammals: the longevity hypothesis. Mol Biol Evol. 25:120-130.
82. Near TJ, Meylan PA, Shaffer HB. 2005. Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles. Am Nat. 165:137-146. (Pubitemid 40263656)
83. Nikaido M, Matsuno F, Hamilton H, et al. (11 co-authors). 2001. Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and paraphyly of river dolphins. Proc Natl Acad Sci U S A. 98:7384-7389. (Pubitemid 32567958)
84. Nikolaev SI, Montoya-Burgos JI, Popadin K, Parand L, Margulies EH, Antonarakis SE. 2007. Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements. Proc Natl Acad Sci U S A. 104:20443-20448.
85. Norman JE, Ashley MV. 2000. Phylogenetics of Perissodactyla and tests of the molecular clock. J Mol Evol. 50:11-21. (Pubitemid 30429998)
86. Nylander JAA. 2004. MrModeltest v2. Program distributed by the author. Uppsala (Sweden): Evolutionary Biology Centre, Uppsala University.
87. Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL. 2008. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581-583. (Pubitemid 351256305)
88. Pastene LA, Goto M, Kanda N, et al. (11 co-authors). 2007. Radiation and speciation of pelagic organisms during periods of global warming: the case of the common minke whale, Balaenoptera acutorostrata. Mol Ecol. 16:1481-1500.
89. Philippe H, Lopez P. 2001. On the conservation of protein sequences in evolution. Trends Biochem Sci. 26:414-416. (Pubitemid 32607481)
90. Phillips MJ. 2009. Branch-length estimation bias misleads molecular dating for a vertebrate molecular phylogeny. Gene 441:132-140.
91. Pulquério MJF, Nichols RA. 2006. Dates from the molecular clock: how wrong can we be? Trends Ecol Evol. 122:180-184. (Pubitemid 46427950)
92. Rannala B, Yang Z. 2007. Bayesian estimation of species divergence times from multiple loci using multiple calibrations. Sys Biol. 56:453-466.
93. Raup D. 1972. Taxonomic diversity during the Phanerozoic. Science 177:1065-1071.
94. Rosenberger AL. 2002. Platyrrhine paleontology and systematics: the paradigm shifts. In: Hartwig WC, editor. The Primate Fossil Record. Cambridge: Cambridge University Press. p. 151-159.
95. Rutschmann F. 2006. Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times. Div Distrib. 12:35-48.
96. Rutschmann FT, Eriksson K, Salim A, Conti E. 2007. Assessing calibration uncertainty in molecular dating: the assignment of fossils to alternative calibration points. Syst Biol. 56:591-608. (Pubitemid 47171633)
97. Sanderson MJ. 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol. 14:1218-1231. (Pubitemid 27523135)
98. Sanderson MJ. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol. 19:101-109. (Pubitemid 34008052)
99. Sasaki T, Nikaido M, Hamilton H, et al. (11 co-authors). 2005. Mitochondrial phylogenetics and evolution of mysticete whales. Syst Biol. 54:77-90. (Pubitemid 40441164)
100. Slater GJ, Price SA, Santini F, Alfaro ME. 2010. Diversity versus disparity and the radiation of modern cetaceans. Proc R Soc B. 277:3097-3104.
101. Smith SA, Donoghue MJ. 2008. Rates of molecular evolution are linked to life history in flowering plants. Science 322:86.
102. Smith SA, Dunn C. 2008. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24:715-716. (Pubitemid 351321218)
103. Soltis PS, Soltis DE, Savolainen V, Crane PR, Barraclough TG. 2002. Rate heterogeneity among lineages of tracheophytes: integration of molecular and fossil data and evidence for molecular living fossils. Proc Natl Acad Sci U S A. 99:4430-4435. (Pubitemid 34286002)
104. Steeman ME. 2007. Cladistic analysis and a revised classification of fossil and recent mysticetes. Zool J Linn Soc. 150:875-894. (Pubitemid 47220958)
105. Steeman ME, Hebsgaard MB, Fordyce RE, Ho SYW, Rabosky DL, Nielsen R, Rahbek C, Glenner H, Sorenson MV, Willerslev E. 2009. Radiation of extant cetaceans driven by restructuring of oceans. Syst Biol. 58:573-585.
106. Strauss D, Sadler PM. 1989. Classical confidence intervals and Bayesian probability estimates for the ends of local taxon ranges. Math Geol. 21:411-427.
107. Steiper ME, Young NM. 2006. Primate molecular divergence dates. Mol Phylogenet Evol. 41:384-394. (Pubitemid 44428198)
108. *and other methods). Version 4.0. Sunderland (MA): Sinauer Associates.
109. Takai M, Anaya F, Shigehara N, Setoguchi T. 2000. New fossil materials of the earliest new world monkey, Branisella boliviana, and the problem of platyrrhine origins. Am J Phys Anthropol. 111:263-281. (Pubitemid 30080402)
110. Tavaré S, Marshal CR, Will O, Soligo C, Martin RD. 2002. Using the fossil record to estimate the age of the last common ancestor of extant primates. Nature 416:726-729. (Pubitemid 34429146)
111. Theodor JM. 2004. Molecular clock divergence estimates and the fossil record of Cetartiodactyla. J Paleontol. 78:39-44. (Pubitemid 38092724)
112. Thorne JL, Kishino H, Painter IS. 1998. Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol. 51:1647-1657. (Pubitemid 28550989)
113. Townsend JP. 2007. Profiling phylogenetic informativeness. Syst Biol. 56:222-231.
114. Townsend JP, Leuenberger C. 2011. Taxon sampling and the optimal rates of evolution for phylogenetic inference. Syst Biol. 60:358-365.
115. Tsantes CM, Steiper ME. 2009. Age at first reproduction explains rate variation in the strepsirhine molecular Ccock. Proc Natl Acad Sci U S A. 106:18165-18170.
116. Ursing BM, Slack KE, Árnason U. 2000. Subordinal artiodactyls relationships in the light of phylogenetic analysis of 12 mitochondrial protein coding genes. Zool Scr. 29:83-88. (Pubitemid 30448186)
117. Welch JJ, Bininda-Emonds ORP, Bromham L. 2008. Correlates of substitution rate variation in mammalian protein-coding sequences. BMC Evol Biol. 8:53.
118. Wiens JJ, Kuczynski CA, Smith SA, Mulcahy D, Sites JW Jr, Townsend TM, Reeder TW. 2008. Branch length, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. Syst Biol. 57:420-431. (Pubitemid 351882203)
119. Wilkinson RD, Steiper ME, Soligo C, Martin RD, Yang Z, Tavare S. 2011. Dating primate divergences through an integrated analysis of palaeontological and molecular data. Syst Biol. 60:16-31.
120. Woolfit M, Bromham L. 2003. Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol Biol Evol. 20:1545-1555. (Pubitemid 37086670)
121. Wu CI, Li WH. 1985. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A. 82:1741-1745.
122. Xia X, Xie Z, Salemi M, Chen L, Wang Y. 2003. An index of substitution saturation and its application. Mol Phylogenet Evol. 26:1-7. (Pubitemid 36029247)
123. Xiong Y, Brandley MC, Xu S, Zhou K, Yang G. 2009. Seven new dolphin mitochondrial genomes and a time-calibrated phylogeny of whales. BMC Evol Biol. 9:20.
124. Yang Z. 1996. Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol. 11:367-372. (Pubitemid 126381530)
125. Yang Z. 2005. Bayesian inference in molecular phylogenetics. In: Gascuel O, editor. Mathematics of evolution and phylogeny. Oxford: Oxford University Press. p. 63-90.
126. Yang Z, Rannala B. 2006. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol Biol Evol. 23:212-226. (Pubitemid 41785968)
127. Yoder AD, Yang Z. 2000. Estimation of primate speciation dates using local molecular clocks. Mol Biol Evol. 17:1081-1090. (Pubitemid 30419221)
128. Zhou Y, Brinkmann H, Rodrigue N, Lartillot N, Philippe H. 2010. A dirichlet process covarion mixture model and its assessments using posterior predictive discrepancy tests. Mol Biol Evol. 27:371-384.