The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation

Roger, Andrew J; Hug, Laura A

doi:10.1098/rstb.2006.1845

Cited by 180Protist diversity and phylogenyGenomics and Phylogenetic StudiesEvolution and Paleontology Studies

The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation

Open access

Roger, Andrew J, Hug, Laura A·2006·Philosophical Transactions of the Royal Society B: Biological Sciences

DOI 10.1098/rstb.2006.1845PMC PMC1578731

Open this paper in CoChat — free account

Abstract

Determining the relationships among and divergence times for the major eukaryotic lineages remains one of the most important and controversial outstanding problems in evolutionary biology. The sequencing and phylogenetic analyses of ribosomal RNA (rRNA) genes led to the first nearly comprehensive phylogenies of eukaryotes in the late 1980s, and supported a view where cellular complexity was acquired during the divergence of extant unicellular eukaryote lineages. More recently, however, refinements in analytical methods coupled with the availability of many additional genes for phylogenetic analysis showed that much of the deep structure of early rRNA trees was artefactual. Recent phylogenetic analyses of a multiple genes and the discovery of important molecular and ultrastructural phylogenetic characters have resolved eukaryotic diversity into six major hypothetical groups. Yet relationships among these groups remain poorly understood because of saturation of sequence changes on the billion-year time-scale, possible rapid radiations of major lineages, phylogenetic artefacts and endosymbiotic or lateral gene transfer among eukaryotes. Estimating the divergence dates between the major eukaryote lineages using molecular analyses is even more difficult than phylogenetic estimation. Error in such analyses comes from a myriad of sources including: (i) calibration fossil dates, (ii) the assumed phylogenetic tree, (iii) the nucleotide or amino acid substitution model, (iv) substitution number (branch length) estimates, (v) the model of how rates of evolution change over the tree, (vi) error inherent in the time estimates for a given model and (vii) how multiple gene data are treated. By reanalysing datasets from recently published molecular clock studies, we show that when errors from these various sources are properly accounted for, the confidence intervals on inferred dates can be very large. Furthermore, estimated dates of divergence vary hugely depending on the methods used and their assumptions. Accurate dating of divergence times among the major eukaryote lineages will require a robust tree of eukaryotes, a much richer Proterozoic fossil record of microbial eukaryotes assignable to extant groups for calibration, more sophisticated relaxed molecular clock methods and many more genes sampled from the full diversity of microbial eukaryotes.

Integrity signals

Registry

Crossref · 10.1098/rstb.2006.1845

Cites

100 of 100 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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 dates of divergence between taxa are more difficult to establish than the phylogeny.
“However, the dates of divergence between taxa—the time that has elapsed since two species shared a common ancestor—are more difficult to establish than the phylogeny (Roger and Hug, 2006).”
From The Astrobiology Primer v2.0 (2016) · cites this paper as Roger and Hug, 2006

Cases in which Parsimony or Compatibility Methods Will be Positively Misleading
Felsenstein, J. (1978) · Systematic Biology · doi:10.1093/sysbio/27.4.401 · Cited by 3,221 · see citing works
A General Empirical Model of Protein Evolution Derived from Multiple Protein Families Using a Maximum-Likelihood Approach
Whelan, S., & Goldman, N. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003851 · Cited by 2,849 · see citing works
TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing
Schmidt, H. A., Strimmer, K., Vingron, M., & von Haeseler, A. (2002) · Bioinformatics · doi:10.1093/bioinformatics/18.3.502 · Cited by 2,512 · see citing works
Cases in which parsimony or compatibility methods will be positively misleading.
Felsenstein, J. (1978) · Systematic Zoology · doi:10.2307/2412923 · Cited by 2,230 · see citing works
The Comparative Method: Moving Beyond Qualitative and Quantitative Strategies
Ragin, C. C. (2014) · doi:10.1525/9780520957350 · Cited by 2,130 · see citing works
Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach.
Sanderson, M. J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003974 · Cited by 1,977 · see citing works
r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock
Sanderson, M. J. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.301 · Cited by 1,906 · see citing works
A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process
Lartillot, N., & Philippe, H. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh112 · Cited by 1,516 · see citing works
Archean Molecular Fossils and the Early Rise of Eukaryotes
Brocks, J. J., Logan, G. A., Buick, R., & Summons, R. E. (1999) · Science · doi:10.1126/science.285.5430.1033 · Cited by 1,275 · see citing works
A kingdom-level phylogeny of eukaryotes based on combined protein data.
Baldauf, S., Roger, A., Wenk-Siefert, I., & Doolittle, W. (2000) · Science · doi:10.1126/science.290.5493.972 · Cited by 1,243 · see citing works
Self-citation
Evolutionary analysis of <i>Arabidopsis</i> , cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus
Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M., & Penny, D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182432999 · Cited by 1,178 · see citing works
A nonparametric approach to estimating divergence times in the absence of rate constancy.
Sanderson, M. J. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025731 · Cited by 1,156 · see citing works
Prokaryotic Evolution in Light of Gene Transfer
Gogarten, J. P., Doolittle, W. F., & Lawrence, J. G. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004046 · Cited by 986 · see citing works
New Concepts of Kingdoms of Organisms
WHITTAKER, R. H. (1969) · Science · doi:10.1126/science.163.3863.150 · Cited by 965 · see citing works
Divergence time and evolutionary rate estimation with multilocus data.
Thorne, J. L., & Kishino, H. (2002) · Systematic Biology · doi:10.1080/10635150290102456 · Cited by 962 · see citing works
Phylogenetic Methods Come of Age: Testing Hypotheses in an Evolutionary Context
Huelsenbeck, J. P., & Rannala, B. (1997) · Science · doi:10.1126/science.276.5310.227 · Cited by 781 · see citing works
Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision
Graur, D., & Martin, W. (2004) · Trends in Genetics · doi:10.1016/j.tig.2003.12.003 · Cited by 669 · see citing works
Monophyletic Origins of the Metazoa: an Evolutionary Link with Fungi
Wainright, P. O., Hinkle, G., Sogin, M. L., & Stickel, S. K. (1993) · Science · doi:10.1126/science.8469985 · Cited by 653 · see citing works
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403984101 · Cited by 638 · see citing works
Performance of a divergence time estimation method under a probabilistic model of rate evolution.
Kishino, H., Thorne, J. L., & Bruno, W. J. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003811 · Cited by 633 · cited 7× · see citing works
“By contrast, the non-parametric rate smoothing (NPRS; Sanderson 1997), penalized likelihood (PL; Sanderson 2002) and the Bayesian log-normal method (Kishino et al. 2001) are all ‘relaxed’ molecular clock methods that allow the rates of evolution to change over the tree in a smooth manner.”
BackgroundMethodInfluential
Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous
Kolaczkowski, B. D., & Thornton, J. W. (2004) · Nature · doi:10.1038/nature02917 · Cited by 617 · see citing works
Determining Divergence Times of the Major Kingdoms of Living Organisms with a Protein Clock
Doolittle, R. F., Feng, D.-F., Tsang, S., Cho, G., & Little, E. (1996) · Science · doi:10.1126/science.271.5248.470 · Cited by 581 · see citing works
The tree of eukaryotes
Keeling, 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 · see citing works
Self-citation
A molecular timescale of eukaryote evolution and the rise of complex multicellular life
Hedges, S. B., Blair, J. E., Venturi, M. L., & Shoe, J. L. (2004) · BMC Evolutionary Biology · doi:10.1186/1471-2148-4-2 · Cited by 578 · see citing works
Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes
Rodríguez‐Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Löffelhardt, W., Bohnert, H. J., Philippe, H., & Lang, B. F. (2005) · Current Biology · doi:10.1016/j.cub.2005.06.040 · Cited by 559 · see citing works
Microsporidia are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins
Hirt, R. P., Logsdon, J. M., Jr., Healy, B., Dorey, M. W., Doolittle, W. F., & Embley, T. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.580 · Cited by 518 · see citing works
Early evolution and the origin of eukaryotes
Sogin, M. L. (1991) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(05)80192-3 · Cited by 500 · see citing works
An examination of the constancy of the rate of molecular evolution
Langley, C. H., & Fitch, W. M. (1974) · Journal of Molecular Evolution · doi:10.1007/bf01797451 · Cited by 491 · see citing works
Modeling compositional heterogeneity
Foster, P. G. (2004) · Systematic Biology · doi:10.1080/10635150490445779 · Cited by 474 · see citing works
Statistical methods for testing functional divergence after gene duplication
Gu, X. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026080 · Cited by 457 · see citing works
Genome-scale phylogeny and the detection of systematic biases.
Phillips, M. J., Delsuc, F., & Penny, D. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh137 · Cited by 450 · see citing works
Myosin domain evolution and the primary divergence of eukaryotes
Richards, T. A., & Cavalier‐Smith, T. (2005) · Nature · doi:10.1038/nature03949 · Cited by 432 · see citing works
Lateral gene transfer in eukaryotes
Andersson, J. O. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-4539-z · Cited by 430 · see citing works
Nuclear-Encoded, Plastid-Targeted Genes Suggest a Single Common Origin for Apicomplexan and Dinoflagellate Plastids
Fast, N. M., Kissinger, J. C., Roos, D. S., & Keeling, P. J. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003818 · Cited by 418 · see citing works
Determining divergence times with a protein clock: Update and reevaluation
Feng, D.-F., Cho, G. S., & Doolittle, R. F. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.13028 · Cited by 416 · see citing works
Phylogenomics of Eukaryotes: Impact of Missing Data on Large Alignments
Philippe, H., Snell, E. A., Bapteste, E. P., Lopez, P., Holland, P. W. H., & Casañe, D. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh182 · Cited by 398 · see citing works
The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium , Entamoeba , and Mastigamoeba
Bapteste, E. P., Brinkmann, H., Lee, J. A., Moore, D. V., Sensen, C. W., Gordon, P. M. K., Duruflé, L., Gaasterland, T., Lopez, P., Müller, M., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.032662799 · Cited by 376 · see citing works
Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record
Peterson, K. J., & Butterfield, N. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503660102 · Cited by 361 · see citing works
Compositional Bias May Affect Both DNA-Based and Protein-Based Phylogenetic Reconstructions
Foster, P. G., & Hickey, D. A. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006471 · Cited by 337 · see citing works
Heterotachy and long-branch attraction in phylogenetics
Philippe, H., Zhou, Y., Brinkmann, H., Rodrigue, N., & Delsuc, F. (2005) · BMC Evolutionary Biology · doi:10.1186/1471-2148-5-50 · Cited by 336 · see citing works
Rooting the Eukaryote Tree by Using a Derived Gene Fusion
Stechmann, A., & Cavalier‐Smith, T. (2002) · Science · doi:10.1126/science.1071196 · Cited by 335 · see citing works
The real ‘kingdoms’ of eukaryotes
Simpson, A. G. B., & Roger, A. J. (2004) · Current Biology · doi:10.1016/j.cub.2004.08.038 · Cited by 335 · see citing works
Self-citation
A Genome Phylogeny for Mitochondria Among -Proteobacteria and a Predominantly Eubacterial Ancestry of Yeast Nuclear Genes
Esser, C. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh160 · Cited by 324 · see citing works
Phylogeny and Classification of Phylum Cercozoa (Protozoa)
Cavalier‐Smith, T., & Chao, E. E. Y. (2003) · Protist · doi:10.1078/143446103322454112 · Cited by 316 · see citing works
Precision of molecular time estimates
Hedges, S. B., & Kumar, S. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.03.004 · Cited by 289 · see citing works
An Empirical Assessment of Long-Branch Attraction Artefacts in Deep Eukaryotic Phylogenomics
Brinkmann, H., van der Giezen, M., Zhou, Y., de Raucourt, G. P., & Philippe, H. (2005) · Systematic Biology · doi:10.1080/10635150500234609 · Cited by 281 · see citing works
VASE-SHAPED MICROFOSSILS FROM THE NEOPROTEROZOIC CHUAR GROUP, GRAND CANYON: A CLASSIFICATION GUIDED BY MODERN TESTATE AMOEBAE
Porter, S. M., Meisterfeld, R., & Knoll, A. H. (2003) · Journal of Paleontology · doi:10.1017/s0022336000044140 · Cited by 278 · see citing works
VASE-SHAPED MICROFOSSILS FROM THE NEOPROTEROZOIC CHUAR GROUP, GRAND CANYON: A CLASSIFICATION GUIDED BY MODERN TESTATE AMOEBAE
Porter, S. M., Meisterfeld, R., & Knoll, A. H. (2003) · Journal of Paleontology · doi:10.1666/0022-3360(2003)077 · Cited by 259 · see citing works
Early–branching or fast–evolving eukaryotes? An answer based on slowly evolving positions
Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M., & Guyader, H. L. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1130 · Cited by 247 · see citing works
The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes
Nikolaev, S. I., Berney, C., Fahrni, J. F., Bolívar, I., Polet, S., Mylnikov, A. P., Aleoshin, V. V., Petrov, N. B., & Pawlowski, J. W. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308602101 · Cited by 244 · see citing works
Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota)
Simpson, A. G. B. (2003) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.02578-0 · Cited by 232 · see citing works
Molecular dating when rates vary
Welch, J. J., & Bromham, L. D. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.02.007 · Cited by 227 · see citing works
A genomic timescale for the origin of eukaryotes
Hedges, S. B., Chen, H., Kumar, S., Wang, D. Y.-C., Thompson, A. S., & Watanabe, H. (2001) · BMC Evolutionary Biology · doi:10.1186/1471-2148-1-4 · Cited by 225 · see citing works
Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi
de Peer, Y. V., Ali, A. B., & Meyer, A. (2000) · Gene · doi:10.1016/s0378-1119(00)00063-9 · Cited by 210 · see citing works
A Bangiophyte Red Alga from the Proterozoic of Arctic Canada
Butterfield, N. J. F., Knoll, A. H., & Swett, K. (1990) · Science · doi:10.1126/science.11538072 · Cited by 207 · see citing works
Accuracy of Rate Estimation Using Relaxed-Clock Models with a Critical Focus on the Early Metazoan Radiation
Ho, S. Y. W. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi125 · Cited by 190 · cited 4× · see citing works
“…of other significant sources we did not examine, such as the accuracy of the phylogenetic tree used, the error in fossil assignments and dates (Graur & Martin 2004; Reisz & Muller 2004), and the realism of the rate of evolution models (Aris-Brosou & Yang 2003; Ho et al. 2005; Welch et al. 2005).”
MethodResultInfluential
Precision of molecular time estimates
BLAIRHEDGES, S. (2004) · Trends in Genetics · doi:10.1016/s0168-9525(04)00072-1 · Cited by 186 · see citing works
Comprehensive Multigene Phylogenies of Excavate Protists Reveal the Evolutionary Positions of “Primitive” Eukaryotes
Simpson, A. G. B., Inagaki, Y., & Roger, A. J. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj068 · Cited by 178 · see citing works
Self-citation
The root of the eukaryote tree pinpointed
Stechmann, A., & Cavalier‐Smith, T. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00602-x · Cited by 176 · see citing works
On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes
Harper, J., Waanders, E., & Keeling, P. J. (2005) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.63216-0 · Cited by 172 · see citing works
Bayesian Models of Episodic Evolution Support a Late Precambrian Explosive Diversification of the Metazoa
Aris-Brosou, S. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg226 · Cited by 164 · see citing works
Estimating Amino Acid Substitution Models: A Comparison of Dayhoff's Estimator, the Resolvent Approach and a Maximum Likelihood Method
Müller, T., Spang, R., & Vingron, M. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003985 · Cited by 163 · see citing works
Phylogeny of eukaryotes based on ribosomal RNA: Long-branch attraction and models of sequence evolution
Philippe* and, H., & Germot, A. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026362 · Cited by 154 · see citing works
Bayesian Mixture Modeling
Neal, R. M. (1992) · Springer eBooks · doi:10.1007/978-94-017-2219-3_14 · Cited by 146 · see citing works
Problems in the development of an explicit hypothetical phylogeny of the lower eukaryotes
Taylor, F. J. R. (1978) · Biosystems · doi:10.1016/0303-2647(78)90031-x · Cited by 144 · see citing works
Combining Multiple Data Sets in a Likelihood Analysis: Which Models are the Best?
Pupko, T., Huchon, D., Cao, Y., Okada, N., & Hasegawa, M. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004053 · Cited by 140 · see citing works
Gene Replacement of Fructose-1,6-Bisphosphate Aldolase Supports the Hypothesis of a Single Photosynthetic Ancestor of Chromalveolates
Patron, N. J., Rogers, M. B., & Keeling, P. J. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.5.1169-1175.2004 · Cited by 139 · see citing works
Phylogenetic Analysis of the Complete Genome Sequence of Encephalitozoon cuniculi Supports the Fungal Origin of Microsporidia and Reveals a High Frequency of Fast-Evolving Genes
Thomarat, F., Vivar√®s, C., & Gouy, M. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-004-2673-0 · Cited by 136 · see citing works
Extreme differences in rates of molecular evolution of foraminifera revealed by comparison of ribosomal DNA sequences and the fossil record
Pawlowski, J. W., Bolívar, I., Fahrni, J. F., de Vargas, C., Gouy, M., & Zaninetti, L. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025786 · Cited by 133 · see citing works
Molecular phylogeny of the free-living archezoanTrepomonas agilis and the nature of the first eukaryote
Cavalier‐Smith, T., & Chao, E. E. (1996) · Journal of Molecular Evolution · doi:10.1007/bf02202103 · Cited by 127 · see citing works
Origins of microsporidia
Keeling, P. J., & McFadden, G. I. (1998) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01185-2 · Cited by 127 · see citing works
Using multiple interdependency to separate functional from phylogenetic correlations in protein alignments
Tillier, E. R. M., & Lui, T. W. H. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg072 · Cited by 127 · see citing works
Heterotachy and Tree Building: A Case Study with Plastids and Eubacteria
Lockhart, P. J., Novis, P. M., Milligan, B. G., Riden, J., Rambaut, A., & Larkum, T. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj005 · Cited by 125 · see citing works
Reconstructing history with amino acid sequences1
Doolittle, R. F. (1992) · Protein Science · doi:10.1002/pro.5560010201 · Cited by 124 · see citing works
Multiple secondary origins of the anaerobic lifestyle in eukaryotes
Martin Embley, T. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1844 · Cited by 124 · see citing works
Foraminifera and Cercozoa Are Related in Actin Phylogeny: Two Orphans Find a Home?
Keeling, P. J. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003941 · Cited by 122 · see citing works
Likelihood, Parsimony, and Heterogeneous Evolution
Spencer, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi123 · Cited by 120 · see citing works
The troublesome parasites — molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade
Wolters, J. (1991) · Biosystems · doi:10.1016/0303-2647(91)90014-c · Cited by 112 · see citing works
Early origin of foraminifera suggested by SSU rRNA gene sequences
Pawlowski, J. W., Bolívar, I., Fahrni, J. F., Cavalier‐Smith, T., & Gouy, M. (1996) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025605 · Cited by 112 · see citing works
Evolutionary History of “Early-Diverging” Eukaryotes: The Excavate Taxon Carpediemonas is a Close Relative of Giardia1
Simpson, A. G. B., Roger, A. J., Silberman, J. D., Leipe, D. D., Edgcomb, V. P., Jermiin, L. S., Patterson, D. J., & Sogin, M. L. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004000 · Cited by 96 · see citing works
Self-citation
A Novel Polyubiquitin Structure in Cercozoa and Foraminifera: Evidence for a New Eukaryotic Supergroup
Archibald, J. M., Longet, D., Pawlowski, J. W., & Keeling, P. J. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg006 · Cited by 96 · see citing works
Phylogenetic Analysis of Eukaryotes Using Heat-Shock Protein Hsp90
Stechmann, A., & Cavalier‐Smith, T. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-2490-x · Cited by 93 · see citing works
Root of the Eukaryota Tree as Inferred from Combined Maximum Likelihood Analyses of Multiple Molecular Sequence Data
Arisue, N., Hasegawa, M., & Hashimoto, T. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msi023 · Cited by 93 · see citing works
The Potential Value of Indels as Phylogenetic Markers: Position of Trichomonads as a Case Study
Bapteste, E. P., & Philippe, H. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004156 · Cited by 93 · see citing works
Covarion Shifts Cause a Long-Branch Attraction Artifact That Unites Microsporidia and Archaebacteria in EF-1α Phylogenies
Inagaki, Y., Susko, E., Fast, N. M., & Roger, A. J. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh130 · Cited by 93 · see citing works
Self-citation
Eukaryote-specific Domains in Translation Initiation Factors: Implications for Translation Regulation and Evolution of the Translation System
Aravind, L., & Koonin, E. V. (2000) · Genome Research · doi:10.1101/gr.10.8.1172 · Cited by 93 · see citing works
Capsaspora owczarzaki is an independent opisthokont lineage
Ruiz‐Trillo, I., Inagaki, Y., Davis, L. A., Sperstad, S. V., Landfald, B., & Roger, A. J. (2004) · Current Biology · doi:10.1016/j.cub.2004.10.037 · Cited by 86 · see citing works
Self-citation
Molecular Clocks Do Not Support the Cambrian Explosion
Blair, J. E., & Hedges, S. B. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi039 · Cited by 73 · cited 1× · see citing works
“As discussed earlier, it is common in phylogenetic analysis of multiple gene data to simply concatenate genes together into one large alignment and treat this as if it were a single gene (e.g. Douzery et al. 2004; Blair & Hedges 2005; Peterson & Butterfield 2005).”
Background
Inference of the Phylogenetic Position of Oxymonads Based on Nine Genes: Support for Metamonada and Excavata
Hampl, V., Horner, D. S., Dyal, P. L., Kulda, J., Jaroslav Flegr, A., Foster, P. G., & Embley, T. M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi245 · Cited by 67 · see citing works
Gene Transfers from Nanoarchaeota to an Ancestor of Diplomonads and Parabasalids
Andersson, J. O. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh254 · Cited by 60 · see citing works
Acritarchs and microfossils from the Mesoproterozoic Bangemall Group, northwestern Australia
Buick, R., & Knoll, A. H. (1999) · Journal of Paleontology · doi:10.1017/s0022336000040634 · Cited by 57 · see citing works
Testing for Differences in Rates-Across-Sites Distributions in Phylogenetic Subtrees
Susko, E., Inagaki, Y., Field, C., Holder, M., & Roger, A. J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004214 · Cited by 54 · see citing works
Self-citation
Molecular dates for the “cambrian explosion”: The influence of prior assumptions.
Welch, J. J., Fontanillas, E., & Bromham, L. (2005) · Systematic Biology · doi:10.1080/10635150590947212 · Cited by 53 · see citing works
Jumping Genes and Shrinking Genomes ‐ Probing the Evolution of Eukaryotic Photosynthesis with Genomics
Archibald, J. M. (2005) · IUBMB Life · doi:10.1080/15216540500167732 · Cited by 52 · see citing works
Evidence from small-subunit ribosomal RNA sequences for a fungal origin of Microsporidia
Fischer, W., & Palmer, J. D. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.03.031 · Cited by 49 · see citing works
On Inconsistency of the Neighbor-Joining, Least Squares, and Minimum Evolution Estimation When Substitution Processes Are Incorrectly Modeled
Susko, E. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh159 · Cited by 49 · see citing works
The Phylogenetic Position of the Pelobiont Mastigamoeba balamuthi Based on Sequences of rDNA and Translation Elongation Factors EF‐1α and EF‐2
Arisue, N., Hashimoto, T., Lee, J. A., Moore, D. V., Gordon, P. M. K., Sensen, C. W., Gaasterland, T., Hasegawa, M., & Müller, M. (2002) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.2002.tb00332.x · Cited by 39 · see citing works
Biases in Phylogenetic Estimation Can Be Caused by Random Sequence Segments
Susko, E., Spencer, M., & Roger, A. J. (2005) · Journal of Molecular Evolution · doi:10.1007/s00239-004-0352-9 · Cited by 27 · see citing works
Self-citation
Calculating the Evolutionary Rates of Different Genes: A Fast, Accurate Estimator with Applications to Maximum Likelihood Phylogenetic Analysis
Bevan, R. B., Lang, B. F., & Bryant, D. (2005) · Systematic Biology · doi:10.1080/10635150500354829 · Cited by 25 · see citing works
The comparative method for evaluating fossil calibration dates: a reply to Hedges and Kumar
Reisz, R. R., & Müller, J. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.09.004 · Cited by 9 · see citing works

Flagged first, then by citations

Sorted by citations

A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies
Akhoundi, M., Kuhls, K., Cannet, A., Votýpka, J., Marty, P., Delaunay, P., & Séréno, D. (2016) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0004349 · Cited by 1,017 · see citing works
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 · see citing works
Control of mucin-type O-glycosylation: A classification of the polypeptide GalNAc-transferase gene family
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 · see citing works
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 900 · see citing works
New Insights on Classification, Identification, and Clinical Relevance ofBlastocystisspp
Tan, K. S. W. (2008) · Clinical Microbiology Reviews · doi:10.1128/cmr.00022-08 · Cited by 701 · see citing works
Estimating divergence times in large molecular phylogenies
Tamura, K., Battistuzzi, F. U., Billing-Ross, P., Murillo, O. D., Filipski, A., & Kumar, S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213199109 · Cited by 660 · see citing works
Taxon sampling and the accuracy of phylogenetic analyses
(2008) · Journal of Systematics and Evolution · doi:10.3724/sp.j.1002.2008.08016 · Cited by 553 · see citing works
The evolution of RNAi as a defence against viruses and transposable elements
Obbard, D. J., Gordon, K. H. J., Buck, A. H., & Jiggins, F. M. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0168 · Cited by 521 · see citing works
Rocks and clocks: calibrating the Tree of Life using fossils and molecules
Donoghue, P. C. J., & Benton, M. J. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.05.005 · Cited by 413 · see citing works
Paleobiological Perspectives on Early Eukaryotic Evolution
Knoll, A. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016121 · Cited by 394 · see citing works
Marine Protistan Diversity
Caron, D. A., Countway, P. D., Jones, A. C., Kim, D. Y., & Schnetzer, A. (2011) · Annual Review of Marine Science · doi:10.1146/annurev-marine-120709-142802 · Cited by 368 · see citing works
The origin and early evolution of eukaryotes in the light of phylogenomics
Koonin, E. V. (2010) · Genome Biology · doi:10.1186/gb-2010-11-5-209 · Cited by 345 · see citing works
The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records
Peterson, K. J., Cotton, J. A., Gehling, J. G., & Pisani, D. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2233 · Cited by 313 · see citing works
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 · see citing works
Self-citation
Cell evolution and Earth history: stasis and revolution
Cavalier‐Smith, T. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1842 · Cited by 277 · see citing works
Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life
Parfrey, L. W., Grant, J. R., Tekle, Y. I., Lasek‐Nesselquist, E., Morrison, H. G., Sogin, M. L., Patterson, D. J., & Katz, L. A. (2010) · Systematic Biology · doi:10.1093/sysbio/syq037 · Cited by 232 · see citing works
Rooting the tree of life by transition analyses.
Cavalier‐Smith, T. (2006) · Biology Direct · doi:10.1186/1745-6150-1-19 · Cited by 221 · see citing works
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 · see citing works
Early evolution of the Eukaryota
Butterfield, N. J. F. (2014) · Palaeontology · doi:10.1111/pala.12139 · Cited by 219 · see citing works
Predation and eukaryote cell origins: A coevolutionary perspective
Cavalier‐Smith, T. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.10.002 · Cited by 206 · see citing works
Evolution of the Apicomplexa: where are we now?
Morrison, D. A. (2009) · Trends in Parasitology · doi:10.1016/j.pt.2009.05.010 · Cited by 205 · see citing works
Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa
Cavalier‐Smith, T. (2012) · European Journal of Protistology · doi:10.1016/j.ejop.2012.06.001 · Cited by 204 · see citing works
The Proterozoic Record of Eukaryotes
Cohen, P. A., & Macdonald, F. A. (2015) · Paleobiology · doi:10.1017/pab.2015.25 · Cited by 173 · see citing works
Autophagy in protists
Duszenko, M., Ginger, M. L., Brennand, A. E., Gualdrón‐López, M., Colombo, M. I., Coombs, G. H., Coppens, I., Jayabalasingham, B., Langsley, G., de Castro, S. L., et al. (2011) · Autophagy · doi:10.4161/auto.7.2.13310 · Cited by 166 · see citing works
Nucleotide substitution rates for the full set of mitochondrial protein-coding genes in Coleoptera
Pons, J., Ribera, I., Bertranpetit, J., & Balke, M. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2010.02.007 · Cited by 166 · see citing works
Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern Hemisphere inferred from three nuclear data sets
Nie, Z., Wen, J., Azuma, H., Qiu, Y., Sun, H., Meng, Y., Sun, W., & Zimmer, E. A. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2008.06.004 · Cited by 158 · see citing works
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 · see citing works
Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia
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 · see citing works
Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins
Shih, P. M., & Matzke, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305813110 · Cited by 151 · see citing works
Conservation and divergence in plant microRNAs
Jones-Rhoades, M. W. (2011) · Plant Molecular Biology · doi:10.1007/s11103-011-9829-2 · Cited by 147 · see citing works
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 · see citing works
Self-citation
Evolution: Revisiting the Root of the Eukaryote Tree
Roger, A. J., & Simpson, A. G. B. (2009) · Current Biology · doi:10.1016/j.cub.2008.12.032 · Cited by 139 · see citing works
Self-citation
Functional Overlap and Regulatory Links Shape Genetic Interactions between Signaling Pathways
van Wageningen, S., Kemmeren, P., Lijnzaad, P., Margaritis, T., Benschop, J. J., de Castro, I. J., van Leenen, D., Groot Koerkamp, M. J. A., Ko, C. W., Miles, A. J., et al. (2010) · Cell · doi:10.1016/j.cell.2010.11.021 · Cited by 133 · see citing works
The Astrobiology Primer v2.0
Domagal-Goldman, S. D., Wright, K. E., Domagal-Goldman, S. D., Wright, K. E., Adamala, K., Arina de la Rubia, L., Bond, J., Dartnell, L. R., Goldman, A. D., Lynch, K., et al. (2016) · Astrobiology · doi:10.1089/ast.2015.1460 · Cited by 136 · see citing works
“However, the dates of divergence between taxa—the time that has elapsed since two species shared a common ancestor— are more difficult to establish than the phylogeny (Roger and Hug, 2006).”
Evidence for eukaryotic diversification in the ∼1800 million-year-old Changzhougou Formation, North China
Lamb, D., Awramik, S. M., Chapman, D. J., & Zhu, S. (2009) · Precambrian Research · doi:10.1016/j.precamres.2009.05.005 · Cited by 133 · see citing works
A Catalogue of Eukaryotic Transcription Factor Types, Their Evolutionary Origin, and Species Distribution
Weirauch, M. T., & Hughes, T. R. (2011) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-90-481-9069-0_3 · Cited by 127 · see citing works
Autophagy in parasitic protists: Unique features and drug targets
Brennand, A., Gualdrón‐López, M., Coppens, I., Rigden, D. J., Ginger, M. L., & Michels, P. A. M. (2011) · Molecular and Biochemical Parasitology · doi:10.1016/j.molbiopara.2011.02.003 · Cited by 126 · see citing works
Ribosomal frameshifting in decoding antizyme mRNAs from yeast and protists to humans: close to 300 cases reveal remarkable diversity despite underlying conservation
Ivanov, I. P., & Atkins, J. F. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm035 · Cited by 127 · see citing works
Multiple secondary origins of the anaerobic lifestyle in eukaryotes
Martin Embley, T. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1844 · Cited by 124 · see citing works
The changing view of eukaryogenesis – fossils, cells, lineages and how they all come together
Dacks, J., Field, M. C., Buick, R., Eme, L., Gribaldo, S., Roger, A., Brochier-Armanet, C., & Devos, D. P. (2016) · Journal of Cell Science · doi:10.1242/jcs.178566 · Cited by 115 · see citing works
Self-citation
A Hypothesis on the Origin and Evolution of Tubulin
Ludueña, R. F. (2013) · International review of cytology · doi:10.1016/b978-0-12-407699-0.00002-9 · Cited by 113 · see citing works
The Biological Big Bang model for the major transitions in evolution
Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-21 · Cited by 115 · see citing works
Snow ball earth and the split of Streptophyta and Chlorophyta
Becker, B. (2012) · Trends in Plant Science · doi:10.1016/j.tplants.2012.09.010 · Cited by 109 · see citing works
Predation between prokaryotes and the origin of eukaryotes
Davidov, Y., & Jurkevitch, É. (2009) · BioEssays · doi:10.1002/bies.200900018 · Cited by 99 · see citing works
Origin and Diversification of Eukaryotes
Katz, L. A. (2010) · Annual Review of Microbiology · doi:10.1146/annurev-micro-090110-102808 · Cited by 94 · see citing works
Plastid endosymbiosis, genome evolution and the origin of green plants
Stiller, J. W. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.08.002 · Cited by 93 · see citing works
MOLECULAR PALAEOBIOLOGY
PETERSON, K. J., SUMMONS, R. E., & DONOGHUE, P. C. J. (2007) · Palaeontology · doi:10.1111/j.1475-4983.2007.00692.x · Cited by 93 · see citing works
Turning the Crown Upside Down: Gene Tree Parsimony Roots the Eukaryotic Tree of Life
Katz, L. A., Grant, J. R., Parfrey, L. W., & Burleigh, J. G. (2012) · Systematic Biology · doi:10.1093/sysbio/sys026 · Cited by 92 · see citing works
Diversity and Evolution of Algae
Clerck, O. D., Bogaert, K. A., & Leliaert, F. (2012) · Advances in botanical research · doi:10.1016/b978-0-12-391499-6.00002-5 · Cited by 89 · see citing works
RNA Interference – Natural Gene-Based Technology for Highly Specific Pest Control (HiSPeC)
de Andrade, E. C., & Hunter, W. B. (2016) · InTech eBooks · doi:10.5772/61612 · Cited by 86 · see citing works
Order within a mosaic distribution of mitochondrial c‐type cytochrome biogenesis systems?
Allen, J. W. A., Jackson, A., Rigden, D. J., Willis, A. C., Ferguson, S. J., & Ginger, M. (2008) · The FEBS Journal · doi:10.1111/j.1742-4658.2008.06380.x · Cited by 88 · see citing works
Testing for Covarion-like Evolution in Protein Sequences
Wang, H.-C., Spencer, M., Susko, E., & Roger, A. J. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl155 · Cited by 74 · see citing works
Self-citation
Late‐Cenozoic origin and diversification of Chatham Islands endemic plant species revealed by analyses of DNA sequence data
Heenan, P. B., Mitchell, A., de Lange, P., Keeling, J., & Paterson, A. M. (2010) · New Zealand Journal of Botany · doi:10.1080/0028825x.2010.494337 · Cited by 73 · see citing works
A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes
Chernikova, D., Motamedi, S., Csürös, M., Koonin, E. V., & Rogozin, I. B. (2011) · Biology Direct · doi:10.1186/1745-6150-6-26 · Cited by 72 · see citing works
Evolution of the Ras-like small GTPases and their regulators
van Dam, T. J. P., Bos, J. L., & Snel, ‎. (2011) · Small GTPases · doi:10.4161/sgtp.2.1.15113 · Cited by 70 · see citing works
Sterols in a unicellular relative of the metazoans
Kodner, R., Summons, R., Pearson, A., King, N., & Knoll, A. (2008) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0803975105 · Cited by 63 · see citing works
Leishmania: origin, evolution and future since the Precambrian
Tuon, F. F., Neto, V. A., & Amato, V. S. (2008) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2008.00455.x · Cited by 69 · see citing works
Masters of miniaturization: Convergent evolution among interstitial eukaryotes
Rundell, R. J., & Leander, B. S. (2010) · BioEssays · doi:10.1002/bies.200900116 · Cited by 67 · see citing works
Proteases fromEntamoebaspp. and Pathogenic Free-Living Amoebae as Virulence Factors
Serrano‐Luna, J., Piña‐Vázquez, C., Reyes‐López, M., Ortíz-Estrada, G., & de la Garza, M. (2013) · Journal of Tropical Medicine · doi:10.1155/2013/890603 · Cited by 65 · see citing works
Stop the Abuse of Time! Strict Temporal Banding is not the Future of Rank-Based Classifications in Fungi (Including Lichens) and Other Organisms
Lücking, R. (2019) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2019.1650517 · Cited by 67 · see citing works
Recent Fungal Diseases of Crop Plants: Is Lateral Gene Transfer a Common Theme?
Oliver, R. P., & Solomon, P. S. (2008) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-21-3-0287 · Cited by 63 · see citing works
The first eukaryote cell: an unfinished history of contestation
O’Malley, M. A. (2010) · Studies in History and Philosophy of Science Part C Studies in History and Philosophy of Biological and Biomedical Sciences · doi:10.1016/j.shpsc.2010.07.010 · Cited by 62 · see citing works
The influence of body size and net diversification rate on molecular evolution during the radiation of animal phyla
Fontanillas, E., Welch, J. J., Thomas, J. A., & Bromham, L. D. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-95 · Cited by 59 · see citing works
Phylogenomics and diversification of Sordariomycetes
Chen, Y., Su, P., Hyde, K., & Maharachchikumbura, S. S. N. (2023) · Mycosphere · doi:10.5943/mycosphere/14/1/5 · Cited by 58 · see citing works
Autophagy in protists: examples of secondary loss, lineage-specific innovations, and the conundrum of remodeling a single mitochondrion
Rigden, D. J., Michels, P. A. M., & Ginger, M. L. (2009) · Autophagy · doi:10.4161/auto.8838 · Cited by 55 · see citing works
Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach
Rivera, A. S., Pankey, M. S., Plachetzki, D. C., Martin, C. V., Syme, A., Serb, J. M., Omilian, A. R., & Oakley, T. H. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-123 · Cited by 56 · see citing works
A multigene timescale and diversification dynamics of Ciliophora evolution
Fernandes, N. M., & Schrago, C. G. (2019) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2019.106521 · Cited by 55 · see citing works
Distinctive biochemistry in the trypanosome mitochondrial intermembrane space suggests a model for stepwise evolution of the MIA pathway for import of cysteine‐rich proteins
Allen, J. W. A., Ferguson, S. J., & Ginger, M. L. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.07.015 · Cited by 55 · see citing works
Timing the Origins of Multicellular Eukaryotes Through Phylogenomics and Relaxed Molecular Clock Analyses
Sharpe*, S. C., Eme*, L., Brown, M. W., & Roger, A. J. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_1 · Cited by 49 · see citing works
Self-citation
Assembling the spiralian tree of life
Giribet, G., Dunn, C. W., Edgecombe, G. D., Hejnol, A., Martindale, M. Q., & Rouse, G. W. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0006 · Cited by 50 · see citing works
A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer
Rogers, M. B., Watkins, R. F., Harper, J., Durnford, D. G., Gray, M. W., & Keeling, P. J. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-89 · Cited by 48 · see citing works
MicroRNAs and metazoan phylogeny: big trees from little genes
Sperling, E. A., & Peterson, K. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0015 · Cited by 44 · see citing works
Algal affinities of Ediacaran and Cambrian organic-walled microfossils with internal reproductive bodies:Tanariumand other morphotypes
Moczydłowska, M. (2015) · Palynology · doi:10.1080/01916122.2015.1006341 · Cited by 45 · see citing works
A Comparison of Global, Gene-Specific, and Relaxed Clock Methods in a Comparative Genomics Framework: Dating the Polyploid History of Soybean (Glycine max)
Egan, A. N., & Doyle, J. J. (2010) · Systematic Biology · doi:10.1093/sysbio/syq041 · Cited by 45 · see citing works
Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns
Sen, L., Fares, M. A., Liang, B., Gao, L., Wang, B., Wang, T., & Su, Y. (2011) · Biology Direct · doi:10.1186/1745-6150-6-29 · Cited by 44 · see citing works
Phylogenomics for Systematic Biology
Posada, D. (2016) · Systematic Biology · doi:10.1093/sysbio/syw027 · Cited by 44 · see citing works
Cell‐Cell Channels, Viruses, and Evolution
Baluška, F. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04995.x · Cited by 41 · see citing works
Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects
Krauß, V., Thümmler, C., Georgi, F., Lehmann, J., Stadler, P. F., & Eisenhardt, C. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn013 · Cited by 43 · see citing works
Temporal patterns of evolution in the Arctic explored inArtemisiaL. (Asteraceae) lineages of different age
Tkach, N., Hoffmann, M. H., Röser, M., & von Hagen, K. B. (2008) · Plant Ecology & Diversity · doi:10.1080/17550870802331912 · Cited by 39 · see citing works
The Precambrian emergence of animal life: a geobiological perspective
Gaidos, E. J., DuBuc, T. Q., Dunford, M. D., MCANDREW, P., PADILLA‐GAMIÑO, J., STUDER, B., Weersing, K., & Stanley, S. M. (2007) · Geobiology · doi:10.1111/j.1472-4669.2007.00125.x · Cited by 38 · see citing works
The mouth, the anus, and the blastopore—open questions about questionable openings
Hejnol, A., & Martindale, M. Q. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0004 · Cited by 37 · see citing works
Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?
Mackiewicz, P., & Gagat, P. (2014) · Acta Societatis Botanicorum Poloniae · doi:10.5586/asbp.2014.044 · Cited by 38 · see citing works
The origin of a mega-diverse genus: datingBegonia(Begoniaceae) using alternative datasets, calibrations and relaxed clock methods
Goodall-Copestake, W. P., Harris, D. J., & Hollingsworth, P. M. (2009) · Botanical Journal of the Linnean Society · doi:10.1111/j.1095-8339.2009.00948.x · Cited by 35 · see citing works
Mitochondrial genes from 18 angiosperms fill sampling gaps for phylogenomic inferences of the early diversification of flowering plants
Xue, J., Dong, S., Wang, M., Song, T., Zhou, G., Li, Z., de Peer, Y. V., Shao, Z., Wang, W., Chen, M., et al. (2020) · Journal of Systematics and Evolution · doi:10.1111/jse.12708 · Cited by 34 · see citing works
BLASTO: a tool for searching orthologous groups
Zhou, Y., & Landweber, L. F. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm278 · Cited by 34 · see citing works
Histories of molecules: Reconciling the past
O’Malley, M. A. (2015) · Studies in History and Philosophy of Science Part A · doi:10.1016/j.shpsa.2015.09.002 · Cited by 33 · see citing works
Acanthamoeba castellanii Proteases are Capable of Degrading Iron‐Binding Proteins as a Possible Mechanism of Pathogenicity
Rico, G. R., Martínez‐Castillo, M., de la Garza, M., Shibayama, M., & Serrano‐Luna, J. (2015) · Journal of Eukaryotic Microbiology · doi:10.1111/jeu.12215 · Cited by 33 · see citing works
Introduction: how and when did microbes change the world?
Cavalier‐Smith, T., Brasier, M. D., & Embley, T. M. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1847 · Cited by 34 · see citing works
Nitrile Hydratase Genes Are Present in Multiple Eukaryotic Supergroups
Marron, A. O., Akam, M. E., & Walker, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032867 · Cited by 30 · see citing works
Biological disjunction along the West Caledonian fault, New Caledonia: a synthesis of molecular phylogenetics and panbiogeography
Heads, M. (2008) · Botanical Journal of the Linnean Society · doi:10.1111/j.1095-8339.2008.00866.x · Cited by 30 · see citing works
Molecular Data Are Transforming Hypotheses on the Origin and Diversification of Eukaryotes
Tekle, Y. I., Parfrey, L. W., & Katz, L. A. (2009) · BioScience · doi:10.1525/bio.2009.59.6.5 · Cited by 30 · see citing works
Cyanobacterial Evolution: Fresh Insight into Ancient Questions
Shih, P. M. (2015) · Current Biology · doi:10.1016/j.cub.2014.12.046 · Cited by 28 · see citing works
Genomic, phylogenetic, and cell biological insights into metazoan origins
Nichols, S. A., Dayel, M. J., & King, N. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0003 · Cited by 24 · see citing works
Molecular phylogeny and evolution of phenotype in silica‐scaled chrysophyte genus Mallomonas
Čertnerová, D., Čertner, M., & Škaloud, P. (2019) · Journal of Phycology · doi:10.1111/jpy.12882 · Cited by 24 · see citing works
Amber microfossils: On the validity of species concept
Girard, V., & Adl, S. M. (2011) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2010.11.002 · Cited by 24 · see citing works
Evolution of promoter-proximal pausing enabled a new layer of transcription control
Chivu, A. G., Basso, B. A., Abuhashem, A., Leger, M. M., Barshad, G., Rice, E. J., Vill, A. C., Wong, W., Chou, S., Chovatiya, G. L., et al. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01718-y · Cited by 23 · see citing works
RNA interference for the identification of ectoparasite vaccine candidates
Marr, E. J., Sargison, N. D., Nisbet, A. J., & Burgess, S. T. G. (2014) · Parasite Immunology · doi:10.1111/pim.12132 · Cited by 22 · see citing works
Phylogenetic, Functional, and Geological Perspectives on Complex Multicellularity
Knoll, A. H., & Hewitt, D. (2011) · The MIT Press eBooks · doi:10.7551/mitpress/9780262015240.003.0013 · Cited by 24 · see citing works
Gene discovery from a pilot study of the transcriptomes from three diverse microbial eukaryotes: Corallomyxa tenera, Chilodonella uncinata, and Subulatomonas tetraspora
Grant, J. R., Lahr, D. J. G., Rey, F., Burleigh, J., Gordon, J., Knight, R., Molestina, R., & Katz, L. A. (2012) · Protist Genomics · doi:10.2478/prge-2012-0002 · Cited by 28 · see citing works
Critiquing blind dating: the dangers of over-confident date estimates in comparative genomics
Wheat, C. W., & Wahlberg, N. (2013) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2013.07.007 · Cited by 21 · see citing works

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 · see citing works
Self-citation
The new phylogeny of eukaryotes
Philippe, H., Germot, A., & Moreira, D. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00137-4 · Cited by 113 · see citing works
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 · see citing works
An Updated and Comprehensive rRNA Phylogeny of (Crown) Eukaryotes Based on Rate-Calibrated Evolutionary Distances
de Peer, Y. V., Baldauf, S. L., Doolittle, W. F., & Meyer, A. (2000) · Journal of Molecular Evolution · doi:10.1007/s002390010120 · Cited by 148 · see citing works
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 · see citing works

Authors: Roger, A. J., & Hug, L. A.
Affiliations: Canadian Institute for Advanced Research (CA)
ORCID: Roger, Andrew J
Hug, Laura A
Venue: Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher: The Royal Society
Published: 2006-05-08
Volume: 361
Issue: 1470
Pages: 1039-1054
ISSN: 0962-8436 (ISSN-L)
1471-2970
DOI: 10.1098/rstb.2006.1845
PMC: PMC1578731
OpenAlex: W2105487208
Cited by: 180
References: 100
Citations by year: 2026: 2 · 2025: 3 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 4 · 2018: 2 · 2017: 4 · 2016: 10 · 2015: 11 · 2014: 9 · 2013: 9 · 2012: 9
FWCI: 1.99
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations: Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Alfred P. Sloan Foundation
Canadian Institute for Advanced Research
Dalhousie University
Killam Trusts
Canadian Institutes of Health Research (MOP62809)
Natural Sciences and Engineering Research Council of Canada (227085-2005)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
Keywords: eukaryotic phylogeny, eukaryotic diversification, divergence time estimation, molecular clock, ribosomal RNA phylogeny, endosymbiotic gene transfer, horizontal gene transfer, fossil calibration, relaxed molecular clock, eukaryotic origin, cellular complexity
MeSH terms: Eukaryotic Cells, Phylogeny, RNA, Ribosomal, Tetrahydrofolate Dehydrogenase, Thymidylate Synthase, 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

The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks