The origin and evolution of model organisms

Nature Reviews Genetics

Volumn 3, Issue 11, 2002, Pages 838-849

  Hedges, S Blair ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 1;

ADAPTIVE RADIATION; ANALYTIC METHOD; ANGIOSPERM; ANIMAL; ARTIODACTYLA; ASCOMYCETES; BAYES THEOREM; BIOGENESIS; BIOLOGICAL MODEL; CENOZOIC; CYANOBACTERIUM; EUKARYOTE EVOLUTION; EVOLUTION; GENE TRANSFER; GYMNOSPERM; HUMAN; LIVERWORT; MAXIMUM LIKELIHOOD METHOD; MONOPHYLY; MOSS; NONHUMAN; PARAPHYLY; PARSIMONY ANALYSIS; PHYLOGENETIC TREE CONSTRUCTION METHOD; PHYLOGENY; PLANT EVOLUTION; PRECAMBRIAN; PRIORITY JOURNAL; PROKARYOTE; RESEARCH; REVIEW; SPIROCHETE; TAXON;

ANIMALS; ARCHAEA; BACTERIA; CHRONOLOGY; EVOLUTION; FUNGI; HUMANS; MODELS, BIOLOGICAL; PHYLOGENY; PLANTS; PROTOZOA;

ANIMALIA; ARTIODACTYLA; ASCOMYCOTA; BRYOPHYTA; EUKARYOTA; GYMNOSPERMAE; MAGNOLIOPHYTA; PROKARYOTA; SPIROCHAETALES;

EID: 0036846746     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg929     Document Type: Review

References (126)

1. Brenner, S. et al. Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature 366, 265-268 (1993).
2. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877-884 (1999). Reviews how comparative biology methods that use phylogenies and molecular clocks can lead to remarkable insights into the evolution of life.
3. Enard, W. et al. Intra- and interspecific variation in primate gene expression patterns. Science 296, 340-343 (2002).
4. Ingman, M., Kaessmann, H., Pääbo, S. & Gyllensten, U. Mitochondrial genome variation and the origin of modern humans. Nature 408, 708-713 (2000).
5. Hedges, S. B. & Kumar, S. Vertebrate genomes compared. Science 297, 1283-1285 (2002).
6. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87, 4576-4579 (1990)
7. Knoll, A. H. The early evolution of eukaryotes: A geological perspective. Science 256, 622-627 (1992).
8. Schopf, J. W. Microfossils of the early Archean Apex chert: New evidence of the antiquity of life. Science 260, 640-646 (1993).
9. Doolittle, W. F. Phylogenetic classification and the universal tree. Science 284, 2124-2128 (1999). Describes how the finding of large amounts of horizontal gene transfer, as inferred from phylogenetic analyses of sequence data, has reshaped our view of the 'tree of life'.
10. Philippe, H. & Forterre, P. The rooting of the universal tree of life is not reliable, J. Mol. Evol. 49, 509-523 (1999).
11. Margulis, L. Archael-eubacterial mergers in the origin of Eukarya: Phylogenetic classification of life. Proc. Natl. Acad. Sci. USA 93, 1071-1076 (1996).
12. Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734-740 (1997).
13. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: The primary kingdoms Proc. Natl. Acad. Sci. USA 74, 5088-5090 (1977).
14. Hansmann, S. & Martin, W. Phylogeny of 33 ribosomal and six other proteins encoded in an ancient gene cluster that is conserved across prokaryotic genomes: Influence of excluding poorly alignable sites from analysis. Int. J. Syst. Evol. Microbiol. 50, 1655-1663 (2000).
15. Brown, J. R., Douady, C. J., Italia, M. J., Marshall, W. E. & Stanhope, M. J. Universal trees based on large combined protein data sets. Nature Genet. 28, 281-285 (2001).
16. Hedges, S. B. et al. A genomic timescale for the origin of eukaryotes. BMC Evol. Biol. 1, 4 (2001).
17. Wolf, Y. I., Rogozin, I. B., Grishin, N. V., Tatusov, R. L. & Koonin, E. V. Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol. Biol. 1, 8 (2001).
18. Brochier, C., Babteste, E., Moreira, D. & Philippe, H. Eubacterial phylogeny based on translational apparatus proteins. Trends Genet. 18, 1-5 (2002).
19. Matte-Tailliez, O., Brochier, C., Forterre, P. & Philippe, H. Archael phylogeny based on ribosomal proteins. Mol. Biol. Evol. 19, 631-639 (2002).
20. Snel, B. Bork, P. & Huynen, M. A. Genome phylogeny based on gene content. Nature Genet. 21, 108-110 (1999).
21. House, C. H. & Fitz-Gibbon, S. T. Using homolog groups to create a whole-genomic tree of free-living organisms: An update. J. Mol. Evol. 54, 539-547 (2002).
22. Tekaia, F., Lazcano, A. & Dujon, B. The genomic tree as revealed from whole proteome comparisons. Genome Res. 9, 550-557 (1999).
23. Daubin, V., Gouy, M. & Perriere, G. A phylogenomic approach to bacterial phylogeny: Evidence of a core of genes sharing a common history. Genome Res. 12, 1080-1090 (2002).
24. Ragan, M. A. Detection of lateral gene transfer among microbial genomes. Curr. Opin. Genet. Dev. 11, 620-626 (2001).
25. Rivera, M. C. & Lake, J. A. Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257, 74-76 (1992).
26. Cammarano, P., Creti, R., Sanangelentoni, A. M. & Palm, P. The Archaea monophyly issue: A phylogeny of translational elongation factor G(2) sequences inferred from an optimized selection of alignment positions. J. Mol. Evol. 49, 524-537 (1999).
27. Faguy, D. M. & Doolittle, W. F. Genomics: Lessons from the Aeropyrum pernix genome. Curr. Biol. 9, R883-R886 (1999).
28. Tourasse, N. J. & Gouy, M. Accounting for evolutionary rate variation among sequence sites consistently changes universal phylogenies deduced from rRNA and proteincoding genes. Mol. Phylogenet. Evol. 13,159-168 (1999).
29. Katoh, K., Kuma, K. I. & Miyata, T. Genetic algorithmbased maximum-likelihood analysis for molecular phylogeny J. Mol. Evol. 53, 477-484 (2001).
30. Nisbet, E. G. & Sleep, N. H. The habitat and nature of early life. Nature 409, 1083-1091 (2001).
31. Galtier, N., Tourasse, N. & Gouy, M. A nonhyperthermophilic common ancestor to extant life forms. Science 283, 220-221 (1999).
32. Brochier, C. & Philippe, H. A non-hyperthermophilic ancestor for Bacteria. Nature 417, 244 (2002).
33. Daubin, V., Gouy, M. & Perrière, G. Bacterial phylogeny using supertree approach. Genome Informatics 12, 155-164 (2001).
34. Mojzsis, S. J. et al. Evidence for life on Earth before 3,800 million years ago. Nature 384, 55-59 (1996).
35. Fedo, C. M. & Whitehouse, M. J. Metasomatic origin of quartz-pyroxene rock, Akilia, Greenland, and implications for Earth's earliest life. Science 296, 1448-1452 (2002).
36. Schopf, J. W., Kudryavtsev, A. B., Agresti, D. G., Wdowiak, T. J. & Czaja, A. D. Laser-Raman imagery of Earth's earliest fossils. Nature 416, 73-76 (2002).
37. Brasier, M. D. et al. Questioning the evidence for Earth's eadiest fossils. Nature 416, 76-81 (2002). Questions whether the 3.5-Gyr-old microfossils that were found in the Apex Chert rocks, in Australia (reference 8) are life forms. Reference 36 is a rebuttal to this paper and provides additional scrutiny of the same microfossils. These authors concur with one conclusion of reference 37, that the fossils are not of Cyanobacteria, but maintain that they are, nonetheless, fossils of microbes.
38. Kollman, J. M. & Doolittle, R. F. Determining the relative rates of change for prokaryotic and eukaryotic proteins with anciently duplicated paralogs. J. Mol. Evol. 51, 173-181 (2000).
39. Feng, D.-F., Cho, G. & Doolittle, R. F. Determining divergence times with a protein clock: Update and reevaluation. Proc. Natl. Acad. Sci. USA 94, 13028-13033 (1997). An update of the influential 1996 Science paper from the laboratory of Russell Doolittle, one of the first to use large numbers of genes or proteins to date early events in the history of life.
40. Summons, R. E., Jahnke, L. L. Hope, J. M. & Logan, G. A. 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400, 554-557 (1999).
41. Corliss, J. O. in Nature and Human Society: The Quest for a Sustainable World (ed. Raven, P. H.) 130-155 (The National Academy of Sciences, Washington DC, 2000).
42. Margulis, L. Origin of Eukaryotic Cells (Yale University Press, New Haven, Connecticut, 1970).
43. Gupta, R. S. Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among Archaebacteria, Eubacteria, and eukaryotes Microbiol. Mol. Biol. Rev. 62, 1435-1491 (1998). Provides a detailed and often overlooked critique of the evidence bearing on the origin of mitochondria and on the number of symbiotic events (and gene transfers) that occurred in the origin of eukaryotes.
44. Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. & Peattie, D. A. Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science 243, 75-77 (1989).
45. Roger, A, Reconstructing early events in eukaryotic evolution. Am. Nat. 154, S146-S163 (1999).
46. Horner, D. S. & Embley, T. M. Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Mol. Biol. Evol. 18, 1970-1975 (2001).
47. Silberman, J. D. et al. Retortamonad flagellates are closely related to diplomonads: Implications for the history of mitochondrial function in eukaryote evolution Mol. Biol. Evol. 19, 777-786 (2002).
48. Williams, B. A., Hirt, R. P., Lucocq, J. M. & Embley, T. M. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865-869 (2002).
49. Katinka, M. D. et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi Nature 414, 450-453 (2001).
50. Keeling, P. J., Luker, M. A. & Palmer, J. D. Evidence from β-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17, 23-31 (2000).
51. Wang, D. Y.-C., Kumar, S. & Hedges, S. B. Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc. R. Soc. Lond. B Biol. Sci. 266, 163-171 (1999).
52. Baldauf, S. L., Roger, A. J., Wenk-Siefert, I. & Doolittle, W. F. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290, 972-977 (2000).
53. Stechmann, A. & Cavalier-Smith, T. Rooting the eukaryote tree by using gene fusion. Science 297, 89-91 (2002).
54. Moreira, D., LeGuyader, H. & Philippe, H. The origin of red algae and the evolution of chloroplasts. Nature 405, 69-72 (2000). Provides strong evidence from several proteins that red algae and glaucocystophytes (glaucophytes) belong to the plant lineage, supporting a single origin of plastids.
55. Bapteste, E. et al. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba and Mastigamoeba. Proc. Natl. Acad. Sci. USA 99, 1414-1419 (2002).
56. King, N. & Carroll, S. B. A receptor tyrosine kinase from choanoflagellates: Molecular insights into early animal evolution. Proc. Natl. Acad. Sci. USA 98, 15032-15037 (2001).
57. Stillier J. W. Riley, J. & Hall, B. D. Are red algae plants? A critical evaluation of three key molecular data sets. J. Mol. Evol. 52, 527-539 (2001).
58. Nickrent, D. L., Parkinson, C. L., Palmer, J. D. & Duff, R. J. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol. Biol. Evol. 17, 1885-1895 (2000).
59. Chaw, S. M., Parkinson, C. L., Cheng, Y., Vincent, T. M. & Palmer, J. D. Seed plant phylogeny inferred from all three plant genomes: Monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl. Acad. Sci. USA 97, 4086-4091 (2000).
60. Qiu, Y.-L., Cho, Y., Cox, J. C. & Palmer, J. D. The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394, 671-674 (1998).
61. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917-920 (1998).
62. Takezaki, N., Rzhetsky, A. & Nei, M. Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12, 823-833 (1995).
63. Sanderson, M. J. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14, 1218-1231 (1997).
64. Thorne, J. L., Kishino, H. & Painter, I. S. Estimating the rate of evolution of the rate of molecular evolution. Mol. Biol. Evol. 15, 1647-1657 (1998)
65. Kishino, H., Thorne, J. L. & Bruno, W. J. Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol. Biol. Evol. 18, 352-361 (2001).
66. Sanderson, M. J. & Doyle, J. A. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Am. J. Bot. 88, 1499-1516 (2001).
67. Heckman, D. S. et al. Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129-1133 (2001).
68. Magallon, S. & Sanderson, M. J. Absolute diversification rates in angiosperm clades. Evolution 55, 1762-1780 (2001).
69. Martin, W., Gierl, A. & Saedler, H. Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339, 46-48 (1989).
70. Crane, P. R., Friis, E. M. & Pedersen, K. R. The origin and early diversification of angiosperms. Nature 374, 27-33 (1995).
71. Smith, A.B. Systematics and the Fossil Record (Blackwell Scientific, London, 1994).
72. Kenrick, P. & Crane, P. R. The origin and early evolution of plants on land. Nature 389, 33-39 (1997).
73. Kirk, P. M., Cannon, P. F., David, J. C. & Stalpers, J. A. Dictionary of Fungi (CAB International, Surrey, UK, 2001).
74. Redecker, D., Kodner, R. & Graham, L. E. Glomalean fungi from the Ordovician. Science 289, 1920-1921 (2000).
75. Berbee, M. L. & Taylor, J. W. in The Mycota. VIIB. Systematics and Evolution (eds McLaughlin, D. J. & McLaughlin, E.) 229-246 (Springer, New York, 2001).
76. Goffeau, A. et al. Life with 6000 genes, Science 274, 546-567 (1996).
77. Wood, V. et al. The genome sequence of Schizosaccharomyces pombe. Nature 415, 871-880 (2002).
78. Butterfeild, N. J. Bangiomorpha pubescens n. gen., n. sp.: Implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386-404 (2000). Describes the oldest taxonomically resolved eukaryotic group (red algae): it arose 1.2 Gyr ago, and therefore has helped to constrain molecular clocks. The article also discusses the significance of this ancient group for understanding the origin of sex and multicellularity.
79. Forsburg, S. L. The art and design of genetic screens: Yeast. Nature Rev. Genet. 2, 659-668 (2001).
80. Schulte, U., Becker, I., Mewes, H. W. & Mannhaupt, G. Large scale analysis of sequences from Neurospora crassa. J. Biotechnol. 94, 3-13 (2002).
81. Berbee, M. L. The phylogeny of plant and animal pathogens in the Ascomycota. Physiol. Mol. Plant Pathol. 59, 165-187 (2001).
82. May, R. M. in Nature and Human Society the Quest for a Sustainable World (ed. Raven, P. H.) 30-45 (The National Academy of Sciences, Washington DC, 2000).
83. Li,W.-H., Gouy, M., Sharp, P. M., Ohuigin, C. & Yang, Y.-W. Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc. Natl. Acad. Sci. USA 87, 6703-6707 (1990).
84. Murphy, W. J. et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348-2351 (2001). Presents a phylogenetic analysis of the most taxonomically diverse sequence data set for placental mammals.
85. Rosenberg, M. S. & Kumar, S. Incomplete taxon sampling is not a problem for phylogenetic inference. Proc. Natl. Acad. Sci. USA 98, 10751-10756 (2001).
86. Aguinaldo, A, M. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489-493 (1997). An influential paper that describes an analysis of sequences from the small subunit ribosomal RNA gene of animals. As a result, nematodes are placed together with arthropods in a controversial grouping dubbed 'Ecdysozoa' (see also reference 93).
87. Adoutte, A. et al. The new animal phylogeny: Reliability and implications. Proc. Natl. Acad. Sci. USA 97, 4453-4456 (2000).
88. deRosa, R. et al. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399, 772-776 (1999).
89. Manua, M., Kruse, M., Muller, W. E. G. & Parco, Y. L. The comparison of β-thymosin homologues among Metazoa supports an arthropod-nematode clade. J. Mol. Evol. 51, 378-381 (2000).
90. Carroll, S. B., Grenier, J. K. & Weatherbee, S. D. From DNA to Diversity (Blackwell Science, Malden, Massachusetts, 2001).
91. Davidson, E. H. Genomic Regulatory Systems (Academic, San Diego, 2001).
92. Hausdorf, B. Early evolution of the bilateria. Syst. Biol. 49, 130-142 (2000).
93. Blair, J. E., Ikeo, K., Gojobori, T. & Hedges, S. B. The evolutionary position of nematodes. BMC Evol. Biol. 2, 7 (2002).
94. Mushegian, A. R., Garay, J. R., Martin, J. & Liu, L. X. Largescale taxonomic profiling of eukaryotic model organisms: A comparison of orthologous proteins encoded by the human, fly, nematode, and yeast genomes. Genome Res. 8, 590-598 (1998).
95. Easteal, S. & Herbert, G. Molecular evidence from the nuclear genome for the time frame of human evolution. J. Mol. Evol. 44, S121-S132 (1997).
96. Arnason, U., Gullberg, A. Burgeuete, A. S. & Janke, A. Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. Hereditas 133, 217-228 (2001).
97. Stauffer, R. L., Walker, A. Ryder, O. A., Lyons-Weiler, M. & Hedges, S. B. Human and ape molecular clocks and constraints on paleontological hypotheses. J. Hered. 92, 469-474 (2001).
98. Chen, F.-C. & Li, W.-H. Genomic divergences between humans and other hominoids and effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet 68, 444-456 (2001).
99. Leakey, M. G. Feibel, C. S., McDougall, I. & Walker, A. New four-million-year-old hominid species from Kanapoi and Allia Bay, Kenya. Nature 376, 565-571 (1995).
100. Wood, B. Hominid revelations from Chad. Nature 418, 134-135 (2002).
101. Brunet, M. et al. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418, 145-151 (2002).
102. Adkins, R. M., Gelke, E. L., Rowe, D, & Honeycutt, R. L. Molecular phylogeny and divergence time estimates for major rodent groups: Evidence frm multiple genes. Mol. Biol. Evol 18, 777-791 (2001).
103. Kumar, S. & Subramanian, S. Mutation rates in mammalian genomes. Proc. Natl. Acad. Sci. USA 99, 803-808 (2002).
104. Benton, M. J. Vertebrate Palaeontology 452 (Blackwell Science, Oxford, 2000).
105. Hedges, S. B., Parker, P. H., Sibley, C. G. & Kumar, S. Continental breakup and the ordinal diversification of birds and mammals. Nature 381, 226-229 (1996).
106. Archibald, J. D. Fossil evidence for a late Cretaceous origin of "hoofed" mammals Science 272, 1150-1153 (1996).
107. Springer, M. S. et al. Endemic African mammals shake the phylogenetic tree, Nature 388, 61-63 (1997). Sequence analyses define a superorder of mammals, now termed 'Afrotheria', that includes elephants, sea cows, hyraxes, aardvarks, golden moles and elephant shrews. After publication of this paper, tenrecs have also been added to this group. Support for the superorder continues to remain strong.
108. Wray, G. A., Levinton, J. S. & Shapiro, L. H. Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274, 568-573 (1996).
109. Fortey, R. A., Briggs, D. E. G. & Wills, M. A. The Cambrian evolutionary 'explosion': Decoupling cladogenesis from morphological disparity. Biol. J. Linn. Soc. Lon. 57, 13-33 (1996).
110. Valentine, J. W., Jablonski, D. & Erwin, D. H. Fossils, molecules and embryos: New perspectives on the Cambrian explosion. Development 126, 851-859 (1999).
111. Budd, G. E. & Jensen, S. A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. 75, 253-295 (2000).
112. Smith, A. B. & Peterson, K. J. Dating the time of origin of major clades: Molecular clocks and the fossil record. Annu. Rev. Earth Planet. Sci. Lon. 30, 65-88 (2002).
113. Knoll, A. H. in Early Life on Earth (ed. Bengtson, S.) 439-449 (Columbia Univ. Press, New York, 1994).
114. Knoll, A. H. & Carroll, S. B. Early animal evolution: Emerging views from comparative biology and geology, Science 284, 2129-2137 (1999).
115. Hoffman, P. F., Kaufman, A. J., Halverson, G. P. & Schrag, D. P. A Neoproterozoic snowball Earth. Science 281, 1342-1346 (1998).
116. Rasmussen, B., Bengston, S., Fletcher, I. R. & McNaughton, N. J. Discoidal impressions and trace-like fossils more than 1200 million years old. Science 296, 1112-1115 (2002).
117. Nei, M. & Kumar, S. Molecular Evolution and Phylogenetics (Oxford Univ. Press. New York, 2000).
118. Rannala, B. & Yang, Z. Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. J. Mol. Evol. 43, 304-311 (1996).
119. Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783-791 (1985).
120. Zuckerkandl, E. & Pauling, L. in Horizons in Biochemistry (eds Marsha, M. & Pullman, B.) 189-225 (Academic, New York, 1962).
121. Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Mol. Biol. Evol. 19, 101-109 (2002).
122. Brocks, J. J., Logan, G. A., Buick, R. & Summons, R. E. Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033-1036 (1999).
123. Han, T.-M. & Runnegar, B. Megascopic eukaryotic algae from the 2.1 billion-year-old Negaunee iron-formation, Michigan Science 257, 232-235 (1992).
124. Javaux, E. J., Knoll, A. H. & Walter, M. R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66-69 (2001).
125. Wikström, N. Savolainen, V. & Chase, M. W. Evolution of the angiosperms: Calibrating the family tree. Proc. R. Soc. Lond. B Biol. Sci. 268, 2211-2220 (2001).
126. James, T. Y., Porter, D., Leander, C. A., Vilgalys, R. & Longcore, J. E. Molecular phylogenies of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics. Can. J. Bot. 78, 336-350 (2000).