On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 8, 2014, Pages

  Eme, Laura ^a   Sharpe, Susan C ^a   Brown, Matthew W ^b   Roger, Andrew J ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; EUKARYOTE; FOSSIL; GENETICS; PHYLOGENY; PROCEDURES; SPECIES DIFFERENTIATION; STATISTICAL MODEL;

BAYES THEOREM; CLASSIFICATION; EUKARYOTA; FOSSILS; GENETIC SPECIATION; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY;

EID: 84894381498     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016139     Document Type: Article

References (120)

1. Akerborg O, Sennblad B, Lagergren J. 2008. Birth-death prior on phylogeny and speed dating. BMC Evol Biol 8: 77.
2. Aris-Brosou S, Yang Z. 2003. Bayesian models of episodic evolution support a late Precambrian explosive diversification of the Metazoa. Mol Biol Evol 20: 1947-1954.
3. Arisue N, Hasegawa M, Hashimoto T. 2005. Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. Mol Biol Evol 22: 409-420.
4. Baele G, Li WLS, Drummond AJ, Suchard MA, Lemey P. 2013. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30: 239-243.
5. Baldauf SL, Roger AJ,Wenk-Siefert I, Doolittle WF. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972-977.
6. Bapteste E, Brinkmann H, Lee Ja, Moore DV, Sensen CW, Gordon P, Duruflé L, Gaasterland T, Lopez P, Müller M, et al. 2002. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci 99: 1414-1419.
7. Berney C, Pawlowski J. 2006. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc Biol Sci 273: 1867-1872.
8. Blair JE, Hedges SB. 2005. Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22: 2275-2284.
9. Blanquart S, Lartillot N. 2006. A Bayesian compound stochastic process for modeling nonstationary and nonhomogeneous sequence evolution. Mol Biol Evol 23: 2058-2071.
10. Blanquart S, Lartillot N. 2008. A site- and time-heterogeneous model of amino acid replacement. Mol Biol Evol 25: 842-858.
11. Bollback JP. 2002. Bayesian model adequacy and choice in phylogenetics. Mol Biol Evol 19: 1171-1180.
12. Brinkmann H, Burger G, Roger AJ, Gray MW, Lang BF, Rodríguez-Ezpeleta N, Philippe H. 2007. Toward resolving the eukaryotic tree: The phylogenetic positions of jakobids and cercozoans. Curr Biol 17: 1420-1425.
13. Brocks JJ. 1999. Archean molecular fossils and the early rise of eukaryotes. Science 285: 1033-1036.
14. Bromham L, Penny D. 2003. The modern molecular clock. Nat Rev Genet 4: 216-224.
15. Brown MW, Kolisko M, Silberman JD, Roger AJ. 2012. Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22: 1123-1127.
16. Brown MW, Sharpe SC, Silberman JD, Heiss AA, Simpson AG, Roger AJ. 2013. Phylogenomics demonstrate that breviate flagellates are related to opisthokonts and apusomonads. Proc Biol Sci 280: 20131755.
17. Budin K, Philippe H. 1998. New insights into the phylogeny of eukaryotes based on ciliate Hsp70 sequences. Mol Biol Evol 15: 943-956.
18. Buick R, Young A. 2010. Ancient acritarchs. 463: 885-886.
19. Burki F. 2014. The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016147.
20. Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, Jakobsen KS, Pawlowski J. 2007. Phylogenomics reshuffles the eukaryotic supergroups. PloS ONE 2: e790.
21. Burki F, Shalchian-Tabrizi K, Pawlowski J. 2008. Phylogenomics reveals a new "megagroup" including most photosynthetic eukaryotes. Biol Lett 4: 366-369.
22. Burki F, Okamoto N, Pombert J-F, Keeling PJ. 2012. The evolutionary history of haptophytes and cryptophytes: Phylogenomic evidence for separate origins. Proc Biol Sci 279: 2246-2254.
23. Butterfield NJ. 2000. Bangiomorpha pubescens n. gen., n. sp.: Implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26: 386-404.
24. Butterfield NJ. 2005. Probable Proterozoic fungi. Paleobiology 31: 165-182.
25. Cavalier-Smith T. 2010. Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6: 342-345.
26. Davies TJ, Savolainen V, Chase MW, Moat J, Barraclough TG. 2004. Environmental energy and evolutionary rates in flowering plants. Proc Biol Sci 271: 2195-2200.
27. Dentzien-Dias PC, Poinar G Jr, de Figueiredo AEQ, Pacheco ACL, Horn BLD, Schultz CL. 2013. Tapeworm eggs in a 270 million-year-old shark coprolite. PLoS ONE 8: e55007.
28. Derelle R, Lang BF. 2012. Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol Biol Evol 29: 1277-1289.
29. Desmond E, Gribaldo S. 2009. Phylogenomics of sterol synthesis: Insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol Evol 1: 364-381.
30. Douzery EJP, Snell EA, Bapteste E, Delsuc F, Philippe H. 2004. The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci 101: 15386-15391.
31. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88.
32. Felsenstein J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27: 401-410.
33. Fischer WW. 2008. Biogeochemistry: Life before the rise of oxygen. Nature 455: 1051-1052.
34. Glazko GV, Koonin EV, Rogozin IB. 2005.Molecular dating: Ape bones agree with chicken entrails. Trends Genet 21: 89-92.
35. Graur D, Martin W. 2004. Reading the entrails of chickens: Molecular timescales of evolution and the illusion of precision. Trends Genet 20: 80-86.
36. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AGB, Roger AJ. 2009. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups." Proc Natl Acad Sci 106: 3859-3864.
37. Han T, Runnegar B. 1992.Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. Science 257: 232-235.
38. Hedges SB, Kumar S. 2004. Precision of molecular time estimates. Trends Genet 20: 242-247.
39. Hedges SB, Chen H, Kumar S, Wang DY, Thompson AS, Watanabe H. 2001. A genomic timescale for the origin of eukaryotes. BMC Evol Biol 1: 4.
40. Hedges SB, Blair JE, Venturi ML, Shoe JL. 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 4: 2.
41. Ho SYW, Phillips MJ. 2009. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 58: 367-380.
42. Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper A. 2011. Time-dependent rates of molecular evolution. Mol Ecol 20: 3087-3101.
43. Hug LA, Roger AJ. 2007. The impact of fossils and taxon sampling on ancient molecular dating analyses. Mol Biol Evol 24: 1889-1897.
44. 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.
45. Javaux EJ. 2006. Extreme life on Earth-Past, present and possibly beyond. Res Microbiol 157: 37-48.
46. Javaux EJ. 2007. The early eukaryotic fossil record. Adv Exp Med Biol 607: 1-19.
47. Javaux E, Knoll A, Walter M. 2001.Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412: 66-69.
48. Javaux EJ, Knoll AH, Walter M. 2003. Recognizing and interpreting the fossils of early eukaryotes. Orig Life Evol Biosph 33: 75-94.
49. Javaux E, Knoll A, Walter M. 2004. TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology 2: 121-132.
50. Javaux EJ, Marshall CP, Bekker A. 2010. Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463: 934-938.
51. Katz LA, Grant JR, Parfrey LW, Burleigh JG. 2012. Turning the crown upside down: Gene tree parsimony roots the eukaryotic tree of life. Syst Biol 61: 653-660.
52. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW. 2005. The tree of eukaryotes. Trends Ecol Evol 20: 670-676.
53. 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.
54. Knoll AH. 2013. Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb Perspect Biol 6: a016121.
55. Knoll AH, Javaux EJ, Hewitt D, Cohen P. 2006. Eukaryotic organisms in Proterozoic oceans. Philos Trans R Soc Lond B Biol Sci 361: 1023-1038.
56. Koonin EV. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11: 209.
57. Lartillot N, Philippe H. 2004. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21: 1095-1109.
58. Lartillot N, Philippe H. 2006. Computing Bayes factors using thermodynamic integration. Syst Biol 55: 195-207.
59. Lartillot N, Brinkmann H, Philippe H. 2007. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol 7: S4.
60. Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3: A Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286-2288.
61. Le SQ, Gascuel O. 2008. An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307-1320.
62. Le SQ, Gascuel O, Lartillot N. 2008. Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24: 2317-2323.
63. Leiming Y, Xunlai Y, Fanwei M, Jie H. 2005. Protists of the upper Mesoproterozoic Ruyang group in Shanxi Province, China. Precambrian Res 141: 49-66.
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. Linder M, Britton T, Sennblad B. 2011. Evaluation of Bayesian models of substitution rate evolution-Parental guidance versus mutual independence. Syst Biol 60: 329-342.
66. Loken C, Gruner D, Groer L, Peltier R, Bunn N, Craig M, Henriques T, Dempsey J, Yu C-H, Chen J, et al. 2010. SciNet: Lessons learned from building a power-efficient top-20 system and data centre. J Phys Conf Ser 256: 012026.
67. Near TJ, Sanderson MJ. 2004. Assessing the quality of molecular divergence time estimates by fossil calibrations and fossil-based model selection. Philos Trans R Soc Lond B Biol Sci 359: 1477-1483.
68. 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.
69. Nielsen R, Huelsenbeck JP. 2002. Detecting positively selected amino acid sites using posterior predictive P-values. Pac Symp Biocomput 588: 576-588.
70. Ogata Y. 1989. AMonte Carlo method for high dimensional integration. Numerische Mathematik 157: 137-157.
71. Pang K, Tang Q, Schiffbauer JD, Yao J, Yuan X, Wan B, Chen L, Ou Z, Xiao S. 2013. The nature and origin of nucleuslike intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology 11: 499-510.
72. Parfrey LW, Grant J, Tekle YI, Lasek-Nesselquist E, Morrison HG, Sogin ML, Patterson DJ, Katz LA. 2010. Broadly sampled multigene analyses yield awell-resolved eukaryotic tree of life. Syst Biol 59: 518-533.
73. Parfrey LW, Lahr DJG, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci 108: 13624-13629.
74. Parham JF, Irmis RB. 2008. Caveats on the use of fossil calibrations for molecular dating: A comment on Near et al. Am Nat 171: 132-136; author reply 137-140.
75. Parham JF, Donoghue PCJ, Bell CJ, Calway TD, Head JJ, Holroyd Pa, Inoue JG, Irmis RB, Joyce WG, Ksepka DT, et al. 2012. Best practices for justifying fossil calibrations. Syst Biol 61: 346-359.
76. Peterson KJ, Butterfield NJ. 2005. Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc Natl Acad Sci 102: 9547-9552.
77. Philippe H, Germot A, Moreira D. 2000a. The new phylogeny of eukaryotes. Curr Opin Genet Dev 10: 596-601.
78. Philippe H, Lopez P, Brinkmann H, Budin K, Germot A, Laurent J, Moreira D, Müller M, Le Guyader H. 2000b. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc Biol Sci 267: 1213-1221.
79. Porter SM. 2006. The Proterozoic fossil record of heterotrophic eukaryotes. In Neoproterozoic geobiology and paleobiology, pp. 1-21. Springer, New York.
80. Porter SM, Knoll AH. 2000. Testate amoebae in the Neoproterozoic era: Evidence from vase-shaped microfossils in the Chuar group, Grand Canyon. Paleobiology 26: 360-385.
81. Porter S, Meisterfeld R, Knoll A. 2003. Vase-shaped microfossils from the Neoproterozoic Chuar group, Grand Canyon: A classification guided by modern testate amoebae. J Paleont 77: 409-429.
82. Rannala B, Yang Z. 2007. Inferring speciation times under an episodic molecular clock. Syst Biol 56: 453-466.
83. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR. 2008. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455: 1101-1104.
84. Reisz RR, Müller J. 2004.Molecular timescales and the fossil record: A paleontological perspective. Trends Genet 20: 237-241.
85. Richards TA, Cavalier-Smith T. 2005. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436: 1113-1118.
86. Rodrigue N, Philippe H, Lartillot N. 2006. Assessing siteinterdependent phylogenetic models of sequence evolution. Mol Biol Evol 23: 1762-1775.
87. Roger AJ, Hug LA. 2006. The origin and diversification of eukaryotes: Problems with molecular phylogenetics and molecular clock estimation. Philos Trans R Soc Lond B Biol Sci 361: 1039-1054.
88. Roger AJ, Simpson AGB. 2009. Evolution: Revisiting the root of the eukaryote tree. Curr Biol 19: R165-R167.
89. Roger AJ, Sandblom O, Doolittle WF, Philippe H. 1999. An evaluation of elongation factor 1a as a phylogenetic marker for eukaryotes. Mol Biol Evol 16: 218-233.
90. Rogozin IB, Basu MK, Csürös M, Koonin EV. 2009. Analysis of rare genomic changes does not support the unikontbikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes. Genome Biol Evol 1: 99-113.
91. Ronquist F, Klopfstein S, Vilhelmsen L, Schulmeister S, Murray DL, Rasnitsyn AP. 2012. A total-evidence approach to dating with fossils, applied to the early radiation of the hymenoptera. Syst Biol 61: 973-999.
92. Rutschmann F, Eriksson T, Salim KA, Conti E. 2007. Assessing calibration uncertainty in molecular dating: The assignment of fossils to alternative calibration points. Syst Biol 56: 591-608.
93. Samuelsson J, Butterfield NJ. 2001. Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: Stratigraphic and palaeobiological implications. Precambrian Research 107: 235-251.
94. Sanders KL, Lee MSY. 2007. Evaluating molecular clock calibrations using Bayesian analyses with soft and hard bounds. Biol Lett 3: 275-279.
95. Sanderson MJ. 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14: 1218-1231.
96. Sanderson MJ. 2002. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Mol Biol Evol 19: 101-109.
97. Shih PM, Matzke NJ. 2013. Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc Natl Acad Sci 110: 12355-12360.
98. Smith AB, Peterson KJ. 2002. Dating the time of origin of major clades: Molecular clocks and the fossil record. Annu Rev Earth Planet Sci 30: 65-88.
99. Sogin ML. 1991. Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1: 457-463.
100. Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood- based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
101. Stechmann A, Cavalier-Smith T. 2002. Rooting the eukaryote tree by using a derived gene fusion. Science 297: 89-91.
102. Stechmann A, Cavalier-Smith T. 2003a. Phylogenetic analysis of eukaryotes using heat-shock protein Hsp90. J Mol Evol 57: 408-419.
103. Stechmann A, Cavalier-Smith T. 2003b. The root of the eukaryote tree pinpointed. Curr Biol 13: R665-R666.
104. Strother PK, Battison L, Brasier MD, Wellman CH. 2011. Earth's earliest non-marine eukaryotes. Nature 473: 505-509.
105. Summons RE, Walter MR. 1990. Molecular fossils and microfossils of prokaryotes and protists from Proterozoic sediments. Am J Sci 290: 212-244.
106. Summons RE, Bradley AS, Jahnke LL, Waldbauer JR. 2006. Steroids, triterpenoids and molecular oxygen. Philos Trans R Soc Lond B Biol Sci 361: 951-968.
107. Takishita K, Chikaraishi Y, Leger MM, Kim E, Yabuki A, Ohkouchi N, Roger AJ. 2012. Lateral transfer of tetrahymanol- synthesizing genes has allowed multiple diverse eukaryote lineages to independently adapt to environments without oxygen. Biol Direct 7: 5.
108. Thorne JL, Kishino H, Painter IS. 1998. Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15: 1647-1657.
109. Van Tuinen M, Hadly EA. 2004. Error in estimation of rate and time inferred from the early amniote fossil record and avian molecular clocks. J Mol Evol 59: 267-276.
110. Waldbauer JR, Sherman LS, Sumner DY, Summons RE. 2009. Late Archean molecular fossils from the Transvaal Supergroup record the antiquity of microbial diversity and aerobiosis. Precambrian Research 169: 28-47.
111. Warnock RCM, Yang Z, Donoghue PCJ. 2012. Exploring uncertainty in the calibration of the molecular clock. Biol Lett 8: 156-159.
112. Welch JJ, Bromham L. 2005. Molecular dating when rates vary. Trends Ecol Evol 20: 320-327.
113. Xie W, Lewis PO, Fan Y, Kuo L, Chen M-H. 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol 60: 150-160.
114. Yang Z. 2006. Computational molecular evolution. Oxford University Press, Oxford.
115. 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.
116. Yin L. 1997. Acanthomorphic acritarchs from Meso-Neoproterozoic shales of the Ruyang group, Shanxi, China. Rev Palaeobot Palynol 98: 15-25.
117. Yoder AD, Yang Z. 2000. Estimation of primate speciation dates using local molecular clocks. Mol Biol Evol 17: 1081-1090.
118. Zhao S, Burki F, Bråte J, Keeling PJ, Klaveness D, Shalchian-Tabrizi K. 2012. Collodictyon-An ancient lineage in the tree of eukaryotes. Mol Biol Evol 29: 1557-1568.
119. Zhongying Z. 1986. Clastic facies microfossils from the Chuanlinggou Formation (1800 Ma) near Jixian, North China. J Micropalaeontology 5: 9-16.
120. Zuckerkandl E, Pauling L. 1965. Evolutionary divergence and convergence in proteins. Evol Genes Proteins 97: 97-166.