Patterns of Diversification in Early Eukaryotes Emmanuelle J

Patterns of diversification in early eukaryotes Emmanuelle J. Javaux

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Emmanuelle J. Javaux. Patterns of diversification in early eukaryotes. Carnets de Geologie, Carnets de Geologie, 2007, CG2007 (M01/06), pp.38-42. hal-00168238

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HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Carnets de Géologie / Notebooks on Geology - Memoir 2007/01, Abstract 06 (CG2007_M01/06) Patterns of diversification in early eukaryotes [Modes de diversification des premiers Eucaryotes]

Emmanuelle J. JAVAUX1

Citation: JAVAUX E.J. (2007).- Patterns of diversification in early eukaryotes. In: STEEMANS P. & JAVAUX E. (eds.), Recent Advances in Palynology.- Carnets de Géologie / Notebooks on Geology, Brest, Memoir 2007/01, Abstract 06 (CG2007_M01/06) Key Words: Proterozoic; early eukaryotes; diversification Mots-Clefs : Protérozoïque ; premiers eucaryotes ; diversification 1 - Introduction Fossils may also record ancestral forms (and steps in evolution) that might not have any The Precambrian includes: the Hadean (4.6 extant relatives. The position of the root of the to 4 Ga), the period of solar system formation tree of life is not yet understood. Within the and Earth accretion; the Archean (4 to 2.5 Ga) eukaryotic tree, the eukaryotes are divided into when life appeared, and the Proterozoic (2.5 to several supergroups whose relationships are not 0.56 Ga) subdivided into the Paleo-, Meso-, and well resolved. Lineages thought to have Neoproterozoic. During this major part of Earth branched early because they seemed to lack history (about 90%), major environmental mitochondria, actually host derived changes were registered in the geological mitochondrial organelles (EMBLEY & MARTIN, record. These events include the step-wise 2006). Nevertheless, calibration of phylogenies oxygenation of the atmosphere and oceans, using dates from fossils, biomarkers, and meteoritic impacts, supercontinent formation isotopes, shows that a major diversification of and breakup, and severe glaciations; they may extant clades occurred in the Neoproterozoic, have had a profound effect on the early preceded by a long evolution of eukaryotic evolution of the eukaryotes. Several lines of fossils starting in the late Archean -as evidence from the geological record, the fossil suggested by biomarkers- or in the late history and molecular phylogenies can be used Paleoproterozoic, when the oldest eukaryotic to decipher the early record of the domain microfossils are found (see reviews in JAVAUX, Eucarya and its evolution. 2006; KNOLL et alii, 2006; PORTER, 2004). Genetic material is rarely preserved in the Superimposing the record of biological rock record, so paleontologists have to rely on innovations and environmental changes on the other features to identify microfossils as fossil record might reveal possible explanations members of the domain Eucarya. Fossils of the pattern of diversification in the middle provide direct evidence of early cells, and Neoproterozoic, long after the origin of the document steps in biological and biochemical domain and possible early divergence of major innovations. Organisms can be preserved by a clades in the Paleo- and Mesoproterozoic when variety of processes in a range of substrates. eukaryotic fossils of unknown biological Early eukaryotic fossils include: carbonaceous affinities are preserved. compressions (the organisms are preserved as As discussed elsewhere (JAVAUX & MARSHALL, a thin film of carbon); acritarchs (organic- 2006; JAVAUX et alii, 2003, 2004; MARSHALL et walled vesicles with unknown biological alii, 2005), in order to determine the biological affinities, they can be extracted from shales affinities of these fossils at the level of domain using strong acids, or observed in thin sections or beyond, we have defined a set of criteria to of shale, chert or phosphorite); multicellular differentiate prokaryotic from eukaryotic organic-walled organisms (chert, shale); vase- microfossils and have formulated a shaped microfossils; molds and casts in methodology combining microscopy and sandstone or shale; skeletons preserved in microchemistry of single acritarchs. Fossils can carbonates or phosphorite; and phylogenetically display morphological and ultrastructural informative molecules (biomarkers and features showing a degree of complexity and/or biopolymers preserved in the rocks that provide particular features unknown in prokaryotic information about past ecosystems and the organisms, therefore pointing to a eukaryotic evolution of biosynthetic pathways). affinity. Indeed, the wall structure and Molecular phylogenies yield important ornamentation, the presence of processes that information or hypotheses about relationships extend from the vesicle wall, the presence of between clades and their order of branching. excystment structures (openings through which However paleobiological data are essential for cyst liberate their content), wall ultrastructure testing these trees and for constraining the and wall chemistry can clarify the biological (minimum age of) timing of diversification. affinities of organic-walled microfossils at the

1 Département de Géologie, Université de Liège, Allée du 6 août, B18, Sart-Tilman, 4000 Liège (Belgium) [email protected] Manuscript online since March 22, 2007

38 Carnets de Géologie / Notebooks on Geology - Memoir 2007/01, Abstract 06 (CG2007_M01/06) level of the domain, and in some cases even at - The bangiophyte red alga Bangiomorpha the level of class. Microchemical analyses such pubescens is so far the oldest taxonomically as micro infra-red and Raman spectroscopy, resolved eukaryote, and records the evolution secondary ion mass spectrometry, and other of complex multicellularity, cell differentiation, techniques applicable to very small samples and sexual reproduction, eukaryotic such as one acritarch can be used to photosynthesis, primary endosymbiosis of a characterize the chemistry of organic chloroplast ancestor by 1.2-1 Ga. Note that microfossils and might even reveal biomolecules these biological innovations are recorded in this specific to extant clades. one fossil population of bangiophyte red algae that chronostratigraphy dates at 1.2 Ga-750 One limitation of this approach is the limited Ma. Chemostratigraphy and lithostratigraphy knowledge that we have about extant indicate an age closer to 1.2 Ga. However other organisms producing fossilizable structures and multicellular photosynthetic eukaryotes also their morphological, ultrastructural and appeared around 1 Ga. chemical properties. This approach requires investigation of preservable biological - Upper Mesoproterozoic / Lower properties and comparative actualistic studies Neoproterozoic rocks (and possibly of taphonomic processes affecting diverse Paleoproterozoic rocks) have yielded organisms in diverse environments (JAVAUX & biomarkers of alveolates (which include MARSHALL, 2006). dinoflagellates and ciliates, among other groups). 2 - The fossil record of biological innovations in early eukaryotes - Palaeovaucheria, a 1 Ga xanthophyte alga, indicates the appearance of stramenopiles Fossils can inform about the evolution of (which include diatoms, xanthophytes, and biological innovations, regardless of their brown algae) and of secondary symbiosis biological affinities, as briefly summarized (involving a red alga-like endosymbiont). below (see reviews in JAVAUX, 2006; KNOLL et - The 750 Ma vase-shaped microfossils alii, 2006 and reference therein). provide a firm calibration point for the - Biomarkers in 2.7 Ga kerogens of the opisthokonts, the clade that includes animals, Fortescue Group, Australia, indicate that fungi and the amoebozoans not to mention contemporaneous cells were able to synthesize direct evidence for heterotrophic eukaryotes sterols, requiring a minimum of oxygen. and eukaryotic biomineralization, and possibly predation. Cladophorales green algae also - Paleo- and Mesoproterozoic macroscopic appeared, recording again multicellular compressions or mold and cast structures have photosynthetic eukaryotes, and implying earlier been compared to algae but this interpretation evolution and diversification of green algae, as remains controversial. clearly underlined by BUTTERFIELD et alii (1994), - The first ornamented acritarchs are KNOLL (2003) and other Precambrian populations of Valeria lophostriata recorded in paleontologists, but recently misunderstood by the Paleoproterozoic of China (~1.8 Ga) and TEYSSÈDRE (2006). Australia (+1.65 Ga). Early Mesoproterozoic - The late Neoproterozoic appearance of acritarchs Shuiyousphaeridium macro- animals preserved as calcareous skeletons reticulatum, Valeria lophostriata, Tappania forming large reefs or as possible animal plana, and Satka favosa exhibits a complexity embryos in phosphorites added another of form observed with TEM, SEM, and light dimension to ecosystems and predation microscopy that is unknown in prokaryotes. pressure. Prokaryotes can be large, they can have ornamentation, and they can have preservable - Florideophyte red algae at ~600 Ma record walls (at least cyanobacterial sheaths), but no the evolution of a tissue-grade organization prokaryote currently known has all three (large (cell differentiation in three dimensions to form size, ornamentation, preservable acid-resistant a tissue with a specific function). walls) at once. Many eukaryotes do. Therefore, these early microfossils display the 3 - Diversity patterns characteristics of a eukaryotic grade of So fossils do provide evidence for the organization, and are interpreted as eukaryotes evolution of eukaryotic biology, but their with a sophisticated cytoskeleton. These 1.65- change in diversity might also tell us something 1.3 Ga fossil assemblages record biological about the factors controlling the patterns we innovations such as reproduction by budding, see in the fossil record. What are those complex ecology, vegetative and resting stages, patterns? synthesis of resistant polymers, synthesis of various wall ornamentation including processes, and a moderate diversity.

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Figure 1: Patterns of early eukaryotic diversification, biological innovations and environmental changes (modified from KNOLL et alii, 2006). This figure shows the general trend of variation in number of eukaryotic taxa (compilation of acritarchs, VSMs, multicellular fossils and macroscopic compressions, data in KNOLL et alii, 2006) through the Proterozoic, and the timing of major environmental changes (supercontinent formation and breakup, widespread glaciations, meteorite impact in Australia, and change in oxygenation), and of biological innovations evidenced by the fossil record (JAVAUX, 2006). 1: Glaciations. 2: Acraman impact.

The Figure 1 is a schematic curve drawn Late Ediacarian, acanthomorphs disappear and from a recent compilation of the number of taxa large leiospheres dominate assemblages. per assemblage throughout the Proterozoic, Cambrian assemblages include a renewed including the acritarchs, the VSMs, multicellular diversity of ornamented forms and small microfossils and macroscopic remains (data and acanthomorphs, generally assumed to references in KNOLL et alii, 2006). Of course, the represent planktonic algal cysts. fossil record is incomplete and more discoveries will undoubtedly improve our understanding. 4 - Controls on diversification Nevertheless, there is a clear trend toward To understand the factors controlling this increasing diversity, starting with a low rate of pattern of fluctuations in diversity, we can diversity in the late Paleoproterozoic, a modest superimpose on the diversity curve, the timing rate in the Mesoproterozoic-early of environmental changes registered in the rock Neoproterozoic, followed by a sharp increase in record and the timing of biological innovations the mid and late Neoproterozoic (or early evinced in the fossil record. Ediacarian). In the late Ediacarian, diversity decreases before rising again at the Three main factors are generally proposed to Phanerozoic boundary. Between "global" explain changes in diversity: genetic glaciations, the fossil record is sparse and innovations, ecological innovations and seems to show a big drop in diversity, although environmental changes. this might also result from insufficient sampling Since early cells had already all the and/or gaps in the fossil record. eukaryotic features typical of their domain by A closer look at the composition of acritarch the late Paleoproterozoic and possibly earlier, assemblages (KNOLL et alii, 2006) reveals that why did diversity stayed modest until the mid- earlier assemblages include mostly smooth and Neoproterozoic? ornamented sphaeromorphs, along with a few Sex, complex multicellularity (and cell forms with asymmetrically distributed processes differentiation) and eukaryotic photosynthesis whereas younger assemblages include more appeared around 1.2 Ga, well before the diversely ornamented acritarchs and acritarchs increase in diversity around 850 Ma. Glaciations with symmetrically distributed processes. In the (poorly constrained at ~720-710 and 650-635

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Ma) and possibly a transient shallow-water "Cambrian explosion") but as pointed out anoxia event at the Precambrian-Cambrian above, cause-and-effects relationships may not boundary might have cut down some of the be so closely connected. Moreover, the authors diversity, but most clades (the red, green, do not explain the rise in diversity around 850 xanthophyte algae, the fungi, and the Ma also detected in their study. amoebae) survived and diversified again in the A multidisciplinary approach combining Phanerozoic. Supercontinent breakup might microscopy and microchemistry on both fossils have increased the surface area of and extant cells may permit a better epicontinental seas and modified the cycle of understanding of the paleobiology of the fossils, nutrients, thus providing new niches and and might clarify this pattern of diversification altering the chemistry of the early oceans. by identifying members of early and later Animal predation pressure might also have clades, such as the late Neoproterozoic played a role in forcing diversification. Some acritarchs (were they animal eggs and/or authors suggested that spines on acritarchs phytoplankton cysts or something else?). One could be a defense mechanism against crucial point to elucidate is whether or not the metazoan grazers, and that the modest early late diversification reflects diversification acritarch diversity could have resulted from the between or within clades. Collating the absence of animals before the Ediacaran paleobiological data with information from (PETERSON & BUTTERFIELD, 2005). However it is geology and geochemistry regarding also possible that some of these acritarchs paleoenvironments and their evolution, and record directly the presence of animals as some with insights from molecular phylogeny, we can of them resemble metazoan eggs (KNOLL et alii, better understand the evolution of life on our 2006), but the wall of at least one species planet and characterize the biosignatures (Tanarium conoideum) was made of a needed for paleobiology and astrobiology. biopolymer similar to algaenan, thus indicating a green algal affinity (MARSHALL et alii, 2005). Acknowledgments Finally in Australia a meteoritic impact (so- called Acraman impact) occurred at ~570 Ma, This extended abstract has benefited from and acritarch assemblages before and after the discussions and/or previous published work in impact seem to differ (GREY, 2005). collaboration with A.H. KNOLL, C.P. MARSHALL, and K. GREY. So far, not any one event seems to explain the observed pattern of early eukaryote Bibliographic references diversification. More precise dating constraints on environmental changes and the fossil record BUTTERFIELD N.J., KNOLL A.H. & SWETT K. (1994).- are needed before drawing conclusions, but Paleobiology of the Neoproterozoic probably the three factors (genetics, ecology, Svanbergjellet Formation, Spitsbergen.- environmental changes) were involved. Fossils and Strata, Oslo, n° 34, 84 p. EMBLEY T. & MARTIN W. (2006).- Eukaryotic 5 - Conclusions evolution, changes and challenges.- Nature, London, vol. 440, n° 7084, p. 623-630. Early eukaryotes had developed many GREY K. (2005).- Ediacaran Palynology of complex and characteristic cellular and Australia.- Memoirs of the Association of molecular mechanisms by 1.2 Ga, but the Australasian Palaeontologists, Canberra, vol. diversity of microscopic forms increased only in 31, 439 p. the middle Neoproterozoic, and a high diversity HUNTLEY J.W., XIAO S. & KOWALENSKI M. (2005).- of macroscopic forms appeared at the end of 1.3 Billion years of acritarch history: An the Proterozoic era. Despite the unavoidable empirical morphospace approach.- incompleteness of the fossil record, the Precambrian Research, Amsterdam, vol. observed pattern seems to reflect natural 144, n° 1-2, p. 52-68. trends. The causes of this relatively late or JAVAUX E.J. (2006).- The early eukaryotic fossil delayed diversification are probably multiple, record. In: JEKELY G. (ed.), Origins and including changes in the chemistry of the early Evolution of Eukaryotic Endomembranes and atmosphere and oceans and a lack of (or Cytoskeleton.- Landes Biosciences, Austin, reduced) predation pressure until the Ediacarian 19 p. when increased oxygenation permitted the JAVAUX E.J., KNOLL A.H. & WALTER M.R. (2003).- evolution of animals (possibly already present) Recognizing and interpreting the fossils of and consequently the complexification of Early Eukaryotes.- Origins of Life and ecosystems (see discussions in PORTER, 2005; Evolution of Biospheres, Amsterdam, vol. PETERSON & BUTTERFIELD, 2005; KNOLL et alii, 33, n° 1, p. 75-94. UNTLEY 2006). H et alii (2006) examined the JAVAUX E.J., KNOLL A.H. & WALTER M.R. (2004).- evolution of variations in the morphology of TEM evidence for eukaryotic diversity in mid- acritarch vesicles, processes, process tips, and Proterozoic oceans.- Geobiology, Malden, ornamentation: broadly correlating the vol. 2, n° 3, p. 121-132. observed pattern with environmental JAVAUX E.J. & MARSHALL C.P. (2006).- A new (glaciations) and ecological changes approach in deciphering early protist (appearance of Ediacaran metazoans and

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paleobiology and evolution: combined Palaeobiology.- Precambrian Research, microscopy and microchemistry of single Amsterdam, vol. 138, n° 3-4, p. 208-224. Proterozoic acritarchs.- Review of PETERSON K.J. & BUTTERFIELD N.J. (2005).- Origin Palaeobotany and Palynology, Amsterdam, of the Eumetazoa: Testing ecological vol. 139, n° 1-4, p. 1-15. predictions of molecular clocks against the KNOLL A.H. (2003).- Life on a young planet. The Proterozoic fossil record.- Proceedings of the first three billion years of evolution on National Academy of Sciences, Washington, Earth.- Princeton University Press, third vol. 102, n° 27, p. 9547-9552. edition, 277 p. PORTER S.M. (2004).- Early eukaryotic KNOLL A.H., JAVAUX E.J., HEWITT D. & COHEN P. diversification. In: LIPPS J. & WAGGONER B. (2006).- Eukaryotic organisms in Proterozoic (eds.), Neoproterozoic-Cambrian biological Oceans.- Philosophical Transactions of the revolutions.- Paleontological Society Papers, Royal Society of London B, London, vol. 361, Lawrence, vol. 10, p. 35-50. n° 1470, p. 1023-1038. TEYSSÈDRE B. (2006).- Are the green algae MARSHALL C.P., JAVAUX E.J., KNOLL A.H. & WALTER (phylum Viridiplantae) two billion years old?- M.R. (2005).- Combined micro-Fourier Carnets de Géologie - Notebooks on transform infrared (FTIR) spectroscopy and Geology, Brest, Article 2006/03 micro-Raman spectroscopy of Proterozoic (CG2006_A03), 15 p. acritarchs: a new approach to