Frameworks for Interpreting the Early Fossil Record of Eukaryotes.

The origin of modern eukaryotes is one of the key transitions in life's history, and also one of the least understood. Although the fossil record provides the most direct view of this process, interpreting the fossils of early eukaryotes and eukaryote-grade organisms is not straightforward. We present two end-member models for the evolution of modern (i.e., crown) eukaryotes-one in which modern eukaryotes evolved early, and another in which they evolved late-and interpret key fossils within these frameworks, including where they might fit in eukaryote phylogeny and what they may tell us about the evolution of eukaryotic cell biology and ecology. Each model has different implications for understanding the rise of complex life on Earth, including different roles of Earth surface oxygenation, and makes different predictions that future paleontological studies can test.

[1]  S. Xiao.  Extinctions, Morphological Gaps, Major Transitions, Stem Groups, and the Origin of Major Clades, with a Focus on Early Animals , 2022, Acta Geologica Sinica - English Edition.

[2]  D. Canfield,et al.  A case for an active eukaryotic marine biosphere during the Proterozoic era , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Natalia N. Ivanova,et al.  A centimeter-long bacterium with DNA contained in metabolically active, membrane-bound organelles , 2022, Science.

[4]  T. Lenton,et al.  Eukaryogenesis and oxygen in Earth history , 2022, Nature Ecology & Evolution.

[5]  E. Javaux,et al.  Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae , 2022, Nature communications.

[6]  Phoebe A. Cohen,et al.  The earliest history of eukaryotic life: uncovering an evolutionary story through the integration of biological and geological data. , 2021, Trends in ecology & evolution.

[7]  Paul E Schavemaker,et al.  The role of mitochondrial energetics in the origin and diversification of eukaryotes , 2021, Nature Ecology & Evolution.

[8]  S. Xiao,et al.  One-billion-year-old epibionts highlight symbiotic ecological interactions in early eukaryote evolution , 2021 .

[9]  E. Turner.  Possible poriferan body fossils in early Neoproterozoic microbial reefs , 2021, Nature.

[10]  N. Planavsky,et al.  Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview , 2021, Astrobiology.

[11]  E. Javaux,et al.  Shale-hosted biota from the Dismal Lakes Group in Arctic Canada supports an early Mesoproterozoic diversification of eukaryotes , 2021, Journal of Paleontology.

[12]  P. Keeling,et al.  Bacterial and archaeal symbioses with protists , 2021, Current Biology.

[13]  P. Donoghue,et al.  The developmental biology of Charnia and the eumetazoan affinity of the Ediacaran rangeomorphs , 2021, Science Advances.

[14]  M. Brasier,et al.  A possible billion-year-old holozoan with differentiated multicellularity , 2021, Current Biology.

[15]  Fabien Burki,et al.  A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids , 2021, Nature Communications.

[16]  P. Donoghue,et al.  Experimental taphonomy of organelles and the fossil record of early eukaryote evolution , 2020, Science Advances.

[17]  R. Rainbird,et al.  High-resolution correlation between contrasting early Tonian carbonate successions in NW Canada highlights pronounced global carbon isotope variations , 2020 .

[18]  Łukasz Lamża.  Superorganisms of the Protist Kingdom: A New Level of Biological Organization , 2020, Foundations of Science.

[19]  D. B. Mills.  The origin of phagocytosis in Earth history , 2020, Interface Focus.

[20]  S. Porter.  Insights into eukaryogenesis from the fossil record , 2020, Interface Focus.

[21]  Thijs J. G. Ettema,et al.  The Archaeal Roots of the Eukaryotic Dynamic Actin Cytoskeleton , 2020, Current Biology.

[22]  S. Xiao,et al.  A one-billion-year-old multicellular chlorophyte , 2020, Nature Ecology & Evolution.

[23]  Takashi Yamaguchi,et al.  Isolation of an archaeon at the prokaryote–eukaryote interface , 2019, Nature.

[24]  E. Javaux,et al.  Early fungi from the Proterozoic era in Arctic Canada , 2019, Nature.

[25]  R. Mann,et al.  The dynamics of stem and crown groups , 2019, Science Advances.

[26]  S. Porter,et al.  Evolution: Ancient Fossilized Amoebae Find Their Home in the Tree , 2019, Current Biology.

[27]  D. Canfield,et al.  Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago , 2019, Proceedings of the National Academy of Sciences.

[28]  E. Javaux,et al.  Organic-walled microfossils from the late Mesoproterozoic to early Neoproterozoic lower Shaler Supergroup (Arctic Canada): Diversity and biostratigraphic significance , 2019, Precambrian Research.

[29]  Maoyan Zhu,et al.  New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China , 2019, Precambrian Research.

[30]  T. Lyons,et al.  Absence of biomarker evidence for early eukaryotic life from the Mesoproterozoic Roper Group: Searching across a marine redox gradient in mid‐Proterozoic habitability , 2019, Geobiology.

[31]  Mark N. Puttick,et al.  Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origins , 2018, Nature Ecology & Evolution.

[32]  A. Bekker,et al.  Triple oxygen isotope evidence for limited mid-Proterozoic primary productivity , 2018, Nature.

[33]  E. Hammarlund.  Valuable snapshots of deep time , 2018, Nature Geoscience.

[34]  Laura Eme,et al.  Archaea and the origin of eukaryotes , 2017, Nature Reviews Microbiology.

[35]  A. Roger,et al.  The Origin and Diversification of Mitochondria , 2017, Current Biology.

[36]  S. Porter,et al.  Vase-shaped microfossil biostratigraphy with new data from Tasmania, Svalbard, Greenland, Sweden and the Yukon , 2017, Precambrian Research.

[37]  L. Yin,et al.  Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton – A window into the early eukaryote evolution , 2017 .

[38]  N. Tosca,et al.  Controlled hydroxyapatite biomineralization in an ~810 million-year-old unicellular eukaryote , 2017, Science Advances.

[39]  C. Marshall.  Five palaeobiological laws needed to understand the evolution of the living biota , 2017, Nature Ecology &Evolution.

[40]  D. Lahr,et al.  Carbonaceous and siliceous Neoproterozoic vase-shaped microfossils (Urucum Formation, Brazil) and the question of early protistan biomineralization , 2017, Journal of Paleontology.

[41]  S. Bengtson,et al.  Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae , 2017, PLoS biology.

[42]  Thijs J. G. Ettema,et al.  Asgard archaea illuminate the origin of eukaryotic cellular complexity , 2017, Nature.

[43]  A. Knoll,et al.  Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution , 2016, Journal of Paleontology.

[44]  S. Porter,et al.  Organic-walled microfossils of the mid-Neoproterozoic Alinya Formation, Officer Basin, Australia , 2016, Journal of Paleontology.

[45]  S. Porter,et al.  Systematics of organic-walled microfossils from the ca. 780–740 Ma Chuar Group, Grand Canyon, Arizona , 2016, Journal of Paleontology.

[46]  A. Knoll,et al.  Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China , 2016, Nature Communications.

[47]  S. Xiao,et al.  A biomechanical analysis of the early eukaryotic fossil Valeria and new occurrence of organic-walled microfossils from the Paleo-Mesoproterozoic Ruyang Group , 2015 .

[48]  Thijs J. G. Ettema,et al.  Complex archaea that bridge the gap between prokaryotes and eukaryotes , 2015, Nature.

[49]  N. Butterfield.  Early evolution of the Eukaryota , 2015 .

[50]  L. Yin,et al.  Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China , 2015, Journal of Paleontology.

[51]  Matthew W. Brown,et al.  On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. , 2014, Cold Spring Harbor perspectives in biology.

[52]  Sylvain Bernard,et al.  The 2.1 Ga Old Francevillian Biota: Biogenicity, Taphonomy and Biodiversity , 2014, PloS one.

[53]  N. Planavsky,et al.  The rise of oxygen in Earth’s early ocean and atmosphere , 2014, Nature.

[54]  Robert S. Sansom,et al.  Fossilization causes organisms to appear erroneously primitive by distorting evolutionary trees , 2013, Scientific Reports.

[55]  Mark C. Field,et al.  Molecular paleontology and complexity in the last eukaryotic common ancestor , 2013, Critical reviews in biochemistry and molecular biology.

[56]  A. Knoll,et al.  Scale Microfossils from the Mid-Neoproterozoic Fifteenmile Group, Yukon Territory , 2012, Journal of Paleontology.

[57]  Daniel J. G. Lahr,et al.  Estimating the timing of early eukaryotic diversification with multigene molecular clocks , 2011, Proceedings of the National Academy of Sciences.

[58]  S. Porter.  The rise of predators , 2011 .

[59]  E. Koonin,et al.  A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes , 2011, Biology Direct.

[60]  A. Knoll.  The Multiple Origins of Complex Multicellularity , 2011 .

[61]  W. Martin,et al.  The energetics of genome complexity , 2010, Nature.

[62]  Philip C. J. Donoghue,et al.  Early life: Origins of multicellularity , 2010, Nature.

[63]  Donald E. Canfield,et al.  Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago , 2010, Nature.

[64]  D. M. Martin,et al.  Horodyskia williamsii new species, a Mesoproterozoic macrofossil from Western Australia , 2010 .

[65]  M. Laan,et al.  The `string of beads' fossil (Horodyskia) in the mid-Proterozoic of Tasmania , 2010 .

[66]  P. Keeling.  The endosymbiotic origin, diversification and fate of plastids , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[67]  C. Marshall,et al.  Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits , 2010, Nature.

[68]  D. Caron,et al.  Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. , 2009, Trends in microbiology.

[69]  S. Gribaldo,et al.  Phylogenomics of Sterol Synthesis: Insights into the Origin, Evolution, and Diversity of a Key Eukaryotic Feature , 2009, Genome biology and evolution.

[70]  S. Awramik,et al.  Evidence for eukaryotic diversification in the ∼1800 million-year-old Changzhougou Formation, North China , 2009 .

[71]  N. Butterfield.  Modes of pre-Ediacaran multicellularity , 2009 .

[72]  Y. Shukla,et al.  Taxonomy and affinity of Early Mesoproterozoic megascopic helically coiled and related fossils from the Rohtas Formation, the Vindhyan Supergroup, India , 2009 .

[73]  Philip M. Novack-Gottshall,et al.  Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity , 2009, Proceedings of the National Academy of Sciences.

[74]  N. Marshall,et al.  Giant Deep-Sea Protist Produces Bilaterian-like Traces , 2008, Current Biology.

[75]  A. Anbar.  Elements and Evolution , 2008, Science.

[76]  S. Xiao,et al.  Silicified Horodyskia and Palaeopascichnus from upper Ediacaran cherts in South China: tentative phylogenetic interpretation and implications for evolutionary stasis , 2008, Journal of the Geological Society.

[77]  S. Bengtson,et al.  The Paleoproterozoic megascopic Stirling biota , 2007 .

[78]  A. Knoll,et al.  Eukaryotic organisms in Proterozoic oceans , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[79]  T. Naganuma,et al.  A haptophyte bearing siliceous scales: ultrastructure and phylogenetic position of Hyalolithus neolepis gen. et sp. nov. (Prymnesiophyceae, Haptophyta). , 2006, Protist.

[80]  Xunlai Yuan,et al.  Protists of the Upper Mesoproterozoic Ruyang Group in Shanxi Province, China , 2005 .

[81]  P. Donoghue.  Saving the stem group—a contradiction in terms? , 2005, Paleobiology.

[82]  A. Knoll,et al.  TEM evidence for eukaryotic diversity in mid‐Proterozoic oceans , 2004 .

[83]  A. Knoll.  Biomineralization and Evolutionary History , 2003 .

[84]  W. F. Cannon,et al.  Age of volcanic rocks and syndepositional iron formations, Marquette Range Supergroup: implications for the tectonic setting of Paleoproterozoic iron formations of the Lake Superior region , 2002 .

[85]  T. Cavalier-smith.  The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. , 2002, International journal of systematic and evolutionary microbiology.

[86]  A. Knoll,et al.  Morphological and ecological complexity in early eukaryotic ecosystems , 2001, Nature.

[87]  J. Pickett-Heaps,et al.  CELL DIVISION AND MORPHOGENESIS OF THE CENTRIC DIATOM CHAETOCEROS DECIPIENS (BACILLARIOPHYCEAE) II. ELECTRON MICROSCOPY AND A NEW PARADIGM FOR TIP GROWTH , 1998 .

[88]  B. Runnegar,et al.  Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. , 1992, Science.

[89]  M. Melkonian,et al.  Scale formation in algae. , 1991, Journal of electron microscopy technique.

[90]  D. Patterson,et al.  The Formation of Siliceous Scales by Raphidiophrys Ambigua (Protista, Centroheliozoa) , 1988 .

[91]  O. Anderson.  Fine Structure of Silica Deposition and the Origin of Shell Components in a Testate Amoeba Netzelia tuberculata , 1988 .

[92]  D. Porter,et al.  DIPLOPHRYS MARINA, A NEW SCALE-FORMING MARINE PROTIST WITH LABYRINTHULID AFFINITIES , 1984 .

[93]  A. Knoll,et al.  Precambrian Eukaryotic Organisms: A Reassessment of the Evidence , 1975, Science.

[94]  A. V. Grimstone,et al.  The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms , 1964, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[95]  E. Javaux,et al.  The Paleoproterozoic fossil record: Implications for the evolution of the biosphere during Earth's middle-age , 2018 .

[96]  A. Knoll.  Paleobiological perspectives on early eukaryotic evolution. , 2014, Cold Spring Harbor perspectives in biology.

[97]  M. Fedonkin,et al.  Middle Proterozoic (1.5 Ga) Horodyskia moniliformis Yochelson and Fedonkin, the oldest known tissue-grade colonial eucaryote , 2002 .

[98]  H. N. Schulz,et al.  Big bacteria. , 2001, Annual review of microbiology.