The DOI matches its Crossref record; 49 of the 50 references it cites were found in a registry or an index.
A molecular timescale of eukaryote evolution and the rise of complex multicellular life
Open accessAbstract
BACKGROUND: The pattern and timing of the rise in complex multicellular life during Earth's history has not been established. Great disparity persists between the pattern suggested by the fossil record and that estimated by molecular clocks, especially for plants, animals, fungi, and the deepest branches of the eukaryote tree. Here, we used all available protein sequence data and molecular clock methods to place constraints on the increase in complexity through time. RESULTS: Our phylogenetic analyses revealed that (i) animals are more closely related to fungi than to plants, (ii) red algae are closer to plants than to animals or fungi, (iii) choanoflagellates are closer to animals than to fungi or plants, (iv) diplomonads, euglenozoans, and alveolates each are basal to plants+animals+fungi, and (v) diplomonads are basal to other eukaryotes (including alveolates and euglenozoans). Divergence times were estimated from global and local clock methods using 20-188 proteins per node, with data treated separately (multigene) and concatenated (supergene). Different time estimation methods yielded similar results (within 5%): vertebrate-arthropod (964 million years ago, Ma), Cnidaria-Bilateria (1,298 Ma), Porifera-Eumetozoa (1,351 Ma), Pyrenomycetes-Plectomycetes (551 Ma), Candida-Saccharomyces (723 Ma), Hemiascomycetes-filamentous Ascomycota (982 Ma), Basidiomycota-Ascomycota (968 Ma), Mucorales-Basidiomycota (947 Ma), Fungi-Animalia (1,513 Ma), mosses-vascular plants (707 Ma), Chlorophyta-Tracheophyta (968 Ma), Rhodophyta-Chlorophyta+Embryophyta (1,428 Ma), Plantae-Animalia (1,609 Ma), Alveolata-plants+animals+fungi (1,973 Ma), Euglenozoa-plants+animals+fungi (1,961 Ma), and Giardia-plants+animals+fungi (2,309 Ma). By extrapolation, mitochondria arose approximately 2300-1800 Ma and plastids arose 1600-1500 Ma. Estimates of the maximum number of cell types of common ancestors, combined with divergence times, showed an increase from two cell types at 2500 Ma to approximately 10 types at 1500 Ma and 50 cell types at approximately 1000 Ma. CONCLUSIONS: The results suggest that oxygen levels in the environment, and the ability of eukaryotes to extract energy from oxygen, as well as produce oxygen, were key factors in the rise of complex multicellular life. Mitochondria and organisms with more than 2-3 cell types appeared soon after the initial increase in oxygen levels at 2300 Ma. The addition of plastids at 1500 Ma, allowing eukaryotes to produce oxygen, preceded the major rise in complexity.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“Indeed, there is a long history of attempts to estimate the timing of animal diversification [40], yielding ages for crown Metazoa that range between 1,298 Ma [41] and 615 Ma [42].”
From Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales (2015) · cites this paper as [41]
The cited source says what the claim attributes to it.
In the citing paper
“The effects this variation could have on molecular clocks, together with frequent disagreement between the ages estimated by way of the fossil record and molecular clocks—especially for the most ancient lineages (Hedges et al., 2004; Donoghue and Benton, 2007)—mean that it may not be possible to produce molecular clocks that can constrain the uncertainty enough to provide any useful information.”
From The Astrobiology Primer v2.0 (2016) · cites this paper as Hedges et al., 2004
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · cited 1×
“Sequences were aligned [ 36 ] and regions of ambiguous alignment were removed when necessary.”
PAML: a program package for phylogenetic analysis by maximum likelihood
Yang, Z. (1997) · Computer applications in the biosciences · doi:10.1093/bioinformatics/13.5.555 · Cited by 5,377 · cited 4×
“Gene-specific and supergene gamma shape parameters (α) were calculated [40] and used for distance and time estimation [45].”
InfluentialMOLECULAR BIOLOGY AND EVOLUTION
(2021) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789811250378_0003 · Cited by 4,434
Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies
Strimmer, K., & von Haeseler, A. (1996) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025664 · Cited by 2,531 · cited 1×
“These concatenated datasets were analyzed using maximum likelihood (JTT + gamma model, quartet puzzling with 1000 steps) [38], minimum evolution (Neighbor-joining, Poisson + gamma model, 2000 bootstraps, complete deletion) [37], and Bayesian Inference (JTT + gamma model, 50,000 generations, 4 chains with starting temp…”
Sanderson, M. J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003974 · Cited by 1,977 · cited 8×
“The SGLPL method was performed in R8S version 1.6 [48] with maximum likelihood branch lengths calculated under a PC+gamma model [40].”
InfluentialA molecular timescale for vertebrate evolution
Kumar, S., & Hedges, S. B. (1998) · Nature · doi:10.1038/31927 · Cited by 1,936 · cited 7×
“Because the coefficient of variation of time estimates is large for small numbers of genes [14], we used a minimum of 20 genes for each divergence.”
InfluentialSelf-citationSanderson, M. J. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.301 · Cited by 1,906 · cited 1×
“6 [48] with maximum likelihood branch lengths calculated under a PC+gamma model [40].”
Molecular Evidence for the Early Colonization of Land by Fungi and Plants
Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L., & Hedges, S. B. (2001) · Science · doi:10.1126/science.1061457 · Cited by 1,020 · cited 2×
“We chose eighteen divergences among major lineages of eukaryotes, including some analyzed previously [24].”
Self-citationVolcanic gases, black smokers, and the great oxidation event
Holland, H. D. (2002) · Geochimica et Cosmochimica Acta · doi:10.1016/s0016-7037(02)00950-x · Cited by 920 · cited 1×
“Organisms with more than 2–3 cell types (the maximum in prokaryotes) appeared relatively early (~2000 Ma), soon after the surface environment became oxygenated at 2300 Ma (Great Oxidation Event; [34]).”
Phylogenetic test of the molecular clock and linearized trees.
Takezaki, N., Rzhetsky, A., & Nei, M. (1995) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040259 · Cited by 826 · cited 1×
“All proteins were tested for rate constancy [45, 46 ]; those rejected at the 5% significance level were excluded from timing analyses.”
Research works printed but not linked: 5
- Huelsenbeck J, Ronquist F: MrBayes Version 3.0. 2003, Uppsala, Sweden, Evolutionary Biology Centre, Uppsala University
- Kumar S: Phyltest: a program for testing phylogenetic hypotheses, ed. 2.0. Institute of Molecular Evolutionary Genetics. 1996, University Park, PA, Pennsylvania State University
- Felsenstein J: PHYLIP version 3.6. 2002, Seattle, Department of Genetics, University of Washington
- Margulis L, Corliss JO, Melkonian M, Chapman DJ: Handbook of Protoctista. 1990, Boston, Massachusetts, Jones and Bartlett, 914-
- Maddison WP, Maddison DR: MacClade. 1992, Sunderland, MA, Sinauer Associates
Cited by
Sorted by citations
Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential
Taylor, M. W., Radax, R., Steger, D., & Wagner, M. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00040-06 · Cited by 1,493
Estimating the timing of early eukaryotic diversification with multigene molecular clocks
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H., & Katz, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110633108 · Cited by 899
The timescale of early land plant evolution
Morris, J. L., Puttick, M. N., Clark, J., Edwards, D., Kenrick, P., Pressel, S., Wellman, C. H., Yang, Z., Schneider, H., & Donoghue, P. C. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719588115 · Cited by 926
Litchman, E., Klausmeier, C. A., Schofield, O., & Falkowski, P. G. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01117.x · Cited by 924
Bennett, E. P., Mandel, U., Clausen, H., Gerken, T. A., Fritz, T. A., & Tabak, L. A. (2012) · Glycobiology · doi:10.1093/glycob/cwr182 · Cited by 876
Phylogeny and Molecular Evolution of the Green Algae
Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F., & Clerck, O. D. (2012) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2011.615705 · Cited by 948
Structural mechanism of plant aquaporin gating
Törnroth‐Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M. E., Tajkhorshid, E., Neutze, R., & Kjellbom, P. O. (2005) · Nature · doi:10.1038/nature04316 · Cited by 863
A Recently Evolved Transcriptional Network Controls Biofilm Development in Candida albicans
Nobile, C. J., Fox, E. P., Nett, J. E., Sorrells, T. R., Mitrovich, Q. M., Hernday, A. D., Tuch, B. B., Andes, D. R., & Johnson, A. D. (2012) · Cell · doi:10.1016/j.cell.2011.10.048 · Cited by 711
Eukaryotic organisms in Proterozoic oceans
Knoll, A. H., Javaux, E. J., Hewitt, D., & Cohen, P. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1843 · Cited by 701
The Genome of the Basidiomycetous Yeast and Human Pathogen Cryptococcus neoformans
Loftus, B., Fung, E., Roncaglia, P., Rowley, D., Amedeo, P., Bruno, D., Vamathevan, J. J., Miranda, M., Anderson, I., Fraser, J. A., et al. (2005) · Science · doi:10.1126/science.1103773 · Cited by 694
Battistuzzi, F. U., Feijao, A., & Hedges, S. B. (2004) · BMC Evolutionary Biology · doi:10.1186/1471-2148-4-44 · Cited by 609
Self-citationKeeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J., & Gray, M. W. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.09.005 · Cited by 579
Xue, B., Dunker, A. K., & Uversky, V. N. (2012) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2012.675145 · Cited by 557
Lifestyles in transition: evolution and natural history of the genus Lactobacillus
Duar, R. M., Lin, X. B., Zheng, J., Martino, M. E., Grenier, T., Pérez-Muñoz, M. E., Leulier, F., Gänzle, M. G., & Walter, J. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux030 · Cited by 567
Ruhfel, B. R., Gitzendanner, M. A., Soltis, P. S., Soltis, P. S., & Burleigh, J. G. (2014) · BMC Evolutionary Biology · doi:10.1186/1471-2148-14-23 · Cited by 560
Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales
dos Reis, M., Thawornwattana, Y., Angelis, K., Telford, M. J., Donoghue, P. C. J., & Yang, Z. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.066 · Cited by 471
Gadagkar, S. R., Rosenberg, M. S., & Kumar, S. (2004) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21026 · Cited by 483
“Consequently , multiple gene and genome sequence datasets can now be used to reconstruct more robust evolutionary relationships (e.g., Delsuc et al., 2003; Hoofer et al., 2003; Teeling et al., 2003; Hedges et al., 2004; Wolf et al., 2004).”
The Origin and Establishment of the Plastid in Algae and Plants
Reyes-Prieto, A., Weber, A. P. M., & Bhattacharya, D. (2007) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130134 · Cited by 453
Evolution of the Rho Family of Ras-Like GTPases in Eukaryotes
Boureux, A., Vignal, E., Faure, S., & Fort, P. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msl145 · Cited by 447
Molecular Phylogeny and Divergence Times of Deuterostome Animals
Blair, J. E., & Hedges, S. B. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi225 · Cited by 451
Self-citationInositol derivatives: evolution and functions
Michell, R. H. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2334 · Cited by 427
Paleobiological Perspectives on Early Eukaryotic Evolution
Knoll, A. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016121 · Cited by 394
Molecular clocks: four decades of evolution
Kumar, S. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1659 · Cited by 422
Assessing the gene space in draft genomes
Parra, G., Bradnam, K., Ning, Z., Keane, T., & Korf, I. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn916 · Cited by 395
Evolution of Inflammatory Diseases
Okin, D. A., & Medzhitov, R. M. (2012) · Current Biology · doi:10.1016/j.cub.2012.07.029 · Cited by 405
Aranda, M., Li, Y., Liew, Y. J., Baumgarten, S., Simakov, O., Wilson, M. C., Piel, J., Ashoor, H., Bougouffa, S., Bajić, V. B., et al. (2016) · Scientific Reports · doi:10.1038/srep39734 · Cited by 388
The Ras protein superfamily: Evolutionary tree and role of conserved amino acids
Rojas, A. M., Fuentes, G., Rausell, A., & Valencia, A. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201103008 · Cited by 406
“Orange numbers in the tree indicate millions of years according to a recently revised scale (Hedges et al., 2004) and the time line is an approximate scale for the purposes of illustration.”
Animal Evolution and the Molecular Signature of Radiations Compressed in Time
Rokas, A., Krüger, D., & Carroll, S. B. (2005) · Science · doi:10.1126/science.1116759 · Cited by 374
Streptophyte algae and the origin of embryophytes
Becker, B., & Marin, B. (2009) · Annals of Botany · doi:10.1093/aob/mcp044 · Cited by 366
Comparative genomics of biotechnologically important yeasts
Riley, R. W., Haridas, S., Wolfe, K. H., Lopes, M., Hittinger, C. T., Göker, M., Salamov, A., Wisecaver, J. H., Long, T. M., Calvey, C. H., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603941113 · Cited by 362
Bourbon, H.-M. G. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn349 · Cited by 371
Establishing a time‐scale for plant evolution
Clarke, J. T., Warnock, R. C. M., & Donoghue, P. C. J. (2011) · New Phytologist · doi:10.1111/j.1469-8137.2011.03794.x · Cited by 353
The genome sequence of the model ascomycete fungus Podospora anserina
Espagne, E., Lespinet, O., Malagnac, F., Silva, C. D., Jaillon, O., Porcel, B. M., Couloux, A., Aury, J., Segurens, B., Poulain, J., et al. (2008) · Genome biology · doi:10.1186/gb-2008-9-5-r77 · Cited by 369
The evolution and diversification of Dicers in plants
Margis, R., Fusaro, A. F., Smith, N. A., Curtin, S. J., WATSON, J. M., Finnegan, E. J., & Waterhouse, P. M. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.03.072 · Cited by 350
Vanderpoorten, A., & Goffinet, B. (2009) · Cambridge University Press eBooks · doi:10.1017/cbo9780511626838 · Cited by 348
Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant
Adir, N. (2005) · Photosynthesis Research · doi:10.1007/s11120-004-2143-y · Cited by 340
Unequal evolutionary conservation of human protein interactions in interologous networks
Brown, K. R., & Jurišica, I. (2007) · Genome biology · doi:10.1186/gb-2007-8-5-r95 · Cited by 349
Dujon, B. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2811 · Cited by 330
Magallón, S., Hilu, K. W., & Quandt, D. (2013) · American Journal of Botany · doi:10.3732/ajb.1200416 · Cited by 321
Choose your partners: dimerization in eukaryotic transcription factors
Amoutzias, G. D., Robertson, D. L., de Peer, Y. V., & Oliver, S. G. (2008) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2008.02.002 · Cited by 297
On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks
Eme, L., Sharpe, S. C., Brown, M. W., & Roger, A. J. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016139 · Cited by 287
Genomic view of the evolution of the complement system
Nonaka, M., & Kimura, A. (2006) · Immunogenetics · doi:10.1007/s00251-006-0142-1 · Cited by 284
Bengtson, S., Sallstedt, T., Belivanova, V., & Whitehouse, M. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2000735 · Cited by 284
Precision of molecular time estimates
Hedges, S. B., & Kumar, S. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.03.004 · Cited by 292
Self-citationA timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic
Kenrick, P., Wellman, C. H., Schneider, H., & Edgecombe, G. D. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0271 · Cited by 274
TCP Transcription Factors Predate the Emergence of Land Plants
Navaud, O., Dabos, P., Carnus, E., Trémousaygue, D., & Hervé, C. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-006-0174-z · Cited by 267
Gene family innovation, conservation and loss on the animal stem lineage
(2018) · doi:10.7554/elife.34226 · Cited by 226
The evolution of WRKY transcription factors
Rinerson, C. I., Rabara, R., Tripathi, P., Shen, Q. J., & Rushton, P. J. (2015) · BMC Plant Biology · doi:10.1186/s12870-015-0456-y · Cited by 263
Exosome Secretion by the Parasitic Protozoan Leishmania within the Sand Fly Midgut
Atayde, V. D., Aslan, H., Townsend, S. E., Hassani, K., Kamhawi, S., & Olivier, M. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.058 · Cited by 251
Lücking, R., Huhndorf, S. M., Pfister, D. H., Plata, E. R., & Lumbsch, H. T. (2009) · Mycologia · doi:10.3852/09-016 · Cited by 232
Protein Family Expansions and Biological Complexity
Vogel, C., & Chothia, C. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020048 · Cited by 227
Gabaldón, T., Rainey, D. Y., & Huynen, M. A. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.02.067 · Cited by 224
Morphological evolution in land plants: new designs with old genes
Pires, N. D., & Dolan, L. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0252 · Cited by 227
Doering, T. L. (2009) · Annual Review of Microbiology · doi:10.1146/annurev.micro.62.081307.162753 · Cited by 220
Calcium-Dependent Protein Kinases in Plants: Evolution, Expression and Function
Valmonte, G. R., Arthur, K., Higgins, C. M., & MacDiarmid, R. M. (2013) · Plant and Cell Physiology · doi:10.1093/pcp/pct200 · Cited by 215
Navarro, N., Neige, P., & Marchand, D. (2005) · Paleobiology · doi:10.1666/0094-8373(2005)031 · Cited by 25
Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis
Gibson, T. M., Shih, P. M., Cumming, V. M., Fischer, W. W., Crockford, P. W., Hodgskiss, M. S. W., Wörndle, S., Creaser, R. A., Rainbird, R. H., Skulski, T. M., et al. (2018) · Geology · doi:10.1130/g39829.1 · Cited by 217
MACROEVOLUTION AND MACROECOLOGY THROUGH DEEP TIME
BUTTERFIELD, N. J. (2007) · Palaeontology · doi:10.1111/j.1475-4983.2006.00613.x · Cited by 267
The relationship between proteome size, structural disorder and organism complexity
Schád, É., Tompa, P., & Hegyi, H. (2011) · Genome biology · doi:10.1186/gb-2011-12-12-r120 · Cited by 221
Early evolution of the Eukaryota
Butterfield, N. J. F. (2014) · Palaeontology · doi:10.1111/pala.12139 · Cited by 225
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196
The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s
Nelson, D. R., Goldstone, J. V., & Stegeman, J. J. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0474 · Cited by 193
Nikoh, N., Tanaka, K., Shibata, F., Kondo, N. I., Hizume, M., Shimada, M., & Fukatsu, T. (2007) · Genome Research · doi:10.1101/gr.7144908 · Cited by 202
Inglis, D. O., Arnaud, M. B., Binkley, J., Shah, P., Skrzypek, M. S., Wymore, F., Binkley, G., Miyasato, S. R., Simison, M., & Sherlock, G. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr945 · Cited by 194
Hanson, A. D., Pribat, A., Waller, J. C., & de Crécy‐Lagard, V. (2009) · Biochemical Journal · doi:10.1042/bj20091328 · Cited by 192
The evolutionary emergence of land plants.
Donoghue, P., Harrison, C. J., Paps, J., & Schneider, H. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.038 · Cited by 153
Dating the Diversification of the Major Lineages of Ascomycota (Fungi)
Prieto, M., & Wedin, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065576 · Cited by 189
Coming of age: orphan genes in plants
Arendsee, Z. W., Li, L., & Wurtele, E. S. (2014) · Trends in Plant Science · doi:10.1016/j.tplants.2014.07.003 · Cited by 185
The many types of carbonic anhydrases in photosynthetic organisms
DiMario, R. J., Machingura, M. C., Waldrop, G. L., & Moroney, J. V. (2017) · Plant Science · doi:10.1016/j.plantsci.2017.12.002 · Cited by 186
Soanes, D. M., Alam, I. S., Cornell, M., Wong, H. M., Hedeler, C., Paton, N. W., Rattray, M., Hubbard, S. J., Oliver, S. G., & Talbot, N. J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002300 · Cited by 184
Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?
Huang, J., & Gogarten, J. P. (2007) · Genome biology · doi:10.1186/gb-2007-8-6-r99 · Cited by 189
Origin and Evolution of Coccolithophores: From Coastal Hunters to Oceanic Farmers
de Vargas, C., Aubry, M., Probert, I., & YOUNG, J. R. (2007) · Elsevier eBooks · doi:10.1016/b978-012370518-1/50013-8 · Cited by 191
Lang, D., Weiche, B., Timmerhaus, G., Richardt, S., Riaño‐Pachón, D. M., Corrêa, L. G. G., Reski, R., Mueller‐Roeber, B., & Rensing, S. A. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq032 · Cited by 189
Reconstructing the evolution of the mitochondrial ribosomal proteome
Smits, P., Smeitink, J. A. M., van den Heuvel, L. P., Huynen, M. A., & Ettema, T. J. G. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm441 · Cited by 187
Chang, Y., Wang, S., Sekimoto, S., Aerts, A. L., Choi, C., Clum, A., LaButti, K. M., Lindquist, E. A., Ngan, C. Y., Ohm, R. A., et al. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv090 · Cited by 185
Hypoxia and Fungal Pathogenesis: To Air or Not To Air?
Grahl, N., Shepardson, K. M., Chung, D., & Cramer, R. A. (2012) · Eukaryotic Cell · doi:10.1128/ec.00031-12 · Cited by 182
Roger, A. J., & Hug, L. A. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1845 · Cited by 180
Hibbett, D. S., & Matheny, P. B. (2009) · BMC Biology · doi:10.1186/1741-7007-7-13 · Cited by 191
Ancient signals: comparative genomics of green plant CDPKs
Hamel, L., Sheen, J., & Séguin, A. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.10.009 · Cited by 177
Hibbett, D. S., Bauer, R., Binder, M., Giachini, A. J., Hosaka, K., Justo, A., Larsson, E., Larsson, K., Lawrey, J. D., Miettinen, O., et al. (2014) · Springer eBooks · doi:10.1007/978-3-642-55318-9_14 · Cited by 176
Reflections on O 2 as a Biosignature in Exoplanetary Atmospheres
Meadows, V. S. (2017) · Astrobiology · doi:10.1089/ast.2016.1578 · Cited by 173
The evolution of plant development
Friedman, W. E., Moore, R. C., & Purugganan, M. D. (2004) · American Journal of Botany · doi:10.3732/ajb.91.10.1726 · Cited by 169
Chen, L., Bush, S. J., Tovar-Corona, J. M., Castillo-Morales, A., & Urrutia, A. O. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu083 · Cited by 173
Classification and functional annotation of eukaryotic protein kinases
Miranda‐Saavedra, D., & Barton, G. J. (2007) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.21444 · Cited by 176
Fungus-like mycelial fossils in 2.4-billion-year-old vesicular basalt
Bengtson, S., Rasmussen, B., Ivarsson, M., Muhling, J. R., Broman, C., Marone, F., Stampanoni, M., & Bekker, A. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0141 · Cited by 165
A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record
Berney, C., & Pawlowski, J. (2006) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2006.3537 · Cited by 212
A meta-analysis of the genomic and transcriptomic composition of complex life
Liu, G., Mattick, J. S., & Taft, R. J. (2013) · Cell Cycle · doi:10.4161/cc.25134 · Cited by 171
Dating the cyanobacterial ancestor of the chloroplast
Falcón, L. I., Magallón, S., & Castillo, A. (2010) · The ISME Journal · doi:10.1038/ismej.2010.2 · Cited by 159
Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity
Doyle, S. M., Shorter, J., Žółkiewski, M., Hoskins, J. R., Lindquist, S. L., & Wickner, S. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1198 · Cited by 156
Evolution of Synapse Complexity and Diversity
Emes, R. D., & Grant, S. G. N. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150433 · Cited by 161
Symbiosis in eukaryotic evolution
López-García, P., Eme, L., & Moreira, D. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.02.031 · Cited by 154
Wever, A. D., Leliaert, F., Verleyen, E., Vanormelingen, P., der Gucht, K. V., Hodgson, D. A., Sabbe, K., & Vyverman, W. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.0994 · Cited by 151
Shaping the mitochondrial proteome
Gabaldón, T., & Huynen, M. A. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.07.011 · Cited by 156
Marine origin of retroviruses in the early Palaeozoic Era
Aiewsakun, P., & Katzourakis, A. (2017) · Nature Communications · doi:10.1038/ncomms13954 · Cited by 152
The impact of fossils and taxon sampling on ancient molecular dating analyses
Hug, L. A., & Roger, A. J. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm115 · Cited by 144
Exploring plant biodiversity: the Physcomitrella genome and beyond
Lang, D., Zimmer, A. D., Rensing, S. A., & Ralf Reski, A. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.07.002 · Cited by 143
Javaux, E., & Knoll, A. H. (2016) · Journal of Paleontology · doi:10.1017/jpa.2016.124 · Cited by 144
Proteomic analysis of the response to high-salinity stress in Physcomitrella patens
Wang, X., Yang, P., Gao, Q., Liu, X., Kuang, T., Shen, S., & He, Y. (2008) · Planta · doi:10.1007/s00425-008-0727-z · Cited by 142
Massive Losses of Taste Receptor Genes in Toothed and Baleen Whales
Feng, P., Zheng, J., Rossiter, S. J., Wang, D., & Zhao, H. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu095 · Cited by 148
Pöggeler, S., & Kück, U. (2006) · Gene · doi:10.1016/j.gene.2006.03.020 · Cited by 137
Metadata
- Authors
- Hedges, S. B., Blair, J. E., Venturi, M. L., & Shoe, J. L.
- Affiliations
- Pennsylvania State University (US)
- Corresponding author
- Hedges, S Blair
- Venue
- BMC Evolutionary Biology
- Published
- 2004-01-28
- Volume
- 4
- Issue
- 1
- Pages
- 2-2
- ISSN
- 1471-2148 (ISSN-L)
- PMC
- PMC341452
- OpenAlex
- W2166647921
- Cited by
- 578
- References
- 50
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 12 · 2023: 15 · 2022: 23 · 2021: 19 · 2020: 22 · 2019: 23 · 2018: 17 · 2017: 33 · 2016: 22 · 2015: 27 · 2014: 31 · 2013: 37 · 2012: 33
- FWCI
- 14.80
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Evolutionary Biology (publishedVersion)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- TUScholarShare (Temple University) (submittedVersion)
- Funders
- National Science Foundation (NNA04CC06A, 0112670, NCC2-1057)
- National Aeronautics and Space Administration (NNA04CC06A)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- eukaryotic evolution, molecular clock, divergence time estimation, red algae, choanoflagellates, diplomonads, alveolates, mitochondrial origin, plastid origin, endosymbiosis
- MeSH terms
- Rhodophyta, Animals, Eukaryotic Cells, Fungi, Phylogeny, Plants, Proteins, Time Factors, Genetic Variation, Vertebrates, Evolution, Molecular
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
