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Paleobiological Perspectives on Early Eukaryotic Evolution

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Paleobiological Perspectives on Early Eukaryotic Evolution Paleobiological Perspectives on Early Eukaryotic Evolution Andrew H. Knoll Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 Correspondence: [email protected] Eukaryotic organisms radiated in Proterozoic oceans with oxygenated surface waters, but, commonly, anoxia at depth. Exceptionally preserved fossils of red algae favor crown group emergence more than 1200 million years ago, but older (up to 1600–1800 million years) microfossils could record stem group eukaryotes. Major eukaryotic diversification 800 million years ago is documented by the increase in the taxonomic richness of complex, organic-walled microfossils, including simple coenocytic and multicellular forms, as well as widespread tests comparable to those of extant testate amoebae and simple foraminiferans and diverse scales comparable to organic and siliceous scales formed today by protists in several clades. Mid-Neoproterozoic establishment or expansion of eukaryophagy provides a possible mechanism for accelerating eukaryotic diversification long after the origin of the domain. Protists continued to diversify along with animals in the more pervasively oxygen- ated oceans of the Phanerozoic Eon. ukaryotic organisms have a long evolution- EXPECTATIONS FROM COMPARATIVE Eary history, recorded, in part, by convention- BIOLOGY al and molecular fossils. For the Phanerozoic Eon (the past 542 million years), eukaryotic The diversity of eukaryotic organisms observ- evolution is richly documented by the skeletons able today makes two sets of predictions for the (and, occasionally, nonskeletal remains) of an- fossil record, one phylogenetic and the other imals, as well as the leaves, stems, roots, and preservational. Phylogenies suggest the relative reproductive organs of land plants. Phylogenet- timing of diversification events through Earth ic logic, however, tells us that eukaryotes must history, and, when incorporated into molecular have a deeper history, one that began long be- clocks, provide quantitative estimates of diver- fore the first plant and animal fossils formed. To gence times. In turn, experimental and obser- what extent does the geological record preserve vational studies of postmortem decay indicate aspects of deep eukaryotic history, and can the that only a subset of eukaryotic clades is likely to chemistry of ancient sedimentary rocks eluci- be represented in the geologic record and these date the environmental conditions under which only under selected environmental circum- the eukaryotic cell took shape? stances. Together, insights into phylogeny and Editors: Patrick J. Keeling and Eugene V. Koonin Additional Perspectives on The Origin and Evolution of Eukaryotes available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a016121 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016121 1 A.H. Knoll preservation provide an empirical guide to pa- mentary accumulations—the White Cliffs of leobiological exploration. Dover, for example, consist mostly of small cal- Molecular sequence comparisons have rev- citic scales made by coccolithophorid algae. olutionized our understanding of evolutionary Tests and scales of calcite and silica document relationships among eukaryotes, but consensus Phanerozoic evolutionary histories for diatoms, on eukaryotic phylogeny remains elusive. Most chrysophytes, coccolithophoids, foraminifer- researchers recognize a limited number of ma- ans, and radiolarians, but do not extend into jor clades, including the opisthonkonts, amoe- Proterozoic rocks (Knoll and Kotrc 2014). Or- bozoans, excavates, plants (sensu lato), and an ganic cell walls, tests, and scales can also survive SAR clade containing the stramenopiles, alveo- bacterial decay, depending on molecular com- lates, and rhizarians (e.g., Katz 2012), and many position, and, in Phanerozoic rocks, these re- recognize the potential for as-yet poorly charac- mains record clades that include dinoflagellates terized taxa to expand that roster (e.g., Patter- and prasinophyte green algae, among other son 1999; Adl et al. 2012). Persistent uncertain- groups. As we shall see, decay-resistant organic ties include the position of the root; placement walls, tests, and scales also document aspects of of groups such as centrohelid heliozoans, hap- Proterozoic protistan evolution, although it can tophytes, and cryptomonads; and both the be challenging to relate preserved fossils to ex- monophyly and relationships of photosynthetic tant clades. lineages commonly grouped as Plantae. Preservation, of course, is not the only hur- Molecular clocks calibrated by phylogenet- dle in paleobiological investigations of Protero- ically well-constrained fossils have been used to zoic rocks. There is also the challenge of recog- estimate the timing of early eukaryotic diversi- nition. In the first instance, how do we identify fication. Choice of algorithm can strongly influ- a fossil as eukaryotic rather than bacterial? ence these estimates (Roger and Hug 2006; Eme Given that the record is one of morphology et al. 2014), but sensitivity tests suggest that for and not DNA or cytology, diagnostic characters a given set of sampled taxa, at least some esti- must be sought in the size, shape, ultrastructure, mates are broadly robust to tree topology and and preservational circumstances of microfos- calibration choices (e.g., Parfrey et al. 2011). sil populations. Eukaryotic cells are commonly Molecular clock estimates generally agree that larger than bacteria and archaeons, but are not much protistan diversification has taken place invariably so. Conversely, cyanobacteria com- during the Phanerozoic Eon, paralleling the di- monly form extracellular sheaths and envelopes versification of animals, plants, and fungi. They that may encompass many cells; this being the also agree on an earlier, Neoproterozoic radia- case, burial can preserve a 100-mm cyanobacte- tion within the major eukaryotic clades, begin- rial envelope that, in life, surrounded numerous ning perhaps 800 million years ago (Mya). micron-scale cells. By itself, then, size is com- Where clocks disagree is on the date for the monly an insufficient criterion for eukaryotic last common ancestor of extant eukaryotes, attribution. Cyst walls associated with resting with some positing a long interval of eukaryotic stages in eukaryotic life cycles commonly have evolution before Neoproterozoic radiation spines or other ornamentation, and they com- (e.g., Hedges et al. 2004; Yoon et al. 2004; Par- monly have acomplex ultrastructure as observed frey et al 2011) and others suggesting a shorter via TEM (e.g., Javaux et al. 2004). Bacteria can fuse (e.g., Douzery et al. 2004; Berney and Paw- have large envelopes (and more rarely cell size) lowski 2006; Chernikova et al. 2011; Shih and (Schultz and Jørgensen 2001), but they rarely if Matzke 2013). The differing predictions of these evercombine large size, ornamented walls, com- clock estimates can be tested against the Prote- plex ultrastructure, and a preservable composi- rozoic fossil record. tion; thus, fossils that display all of these charac- How do protists impart a paleobiological teristics are widely regarded as eukaryotic. signature to sedimentary rocks? Mineralized Molecular fossils provide another means by protistan skeletons can form significant sedi- which eukaryotic organisms can impart a sig- 2 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016121 Paleobiology of Early Eukaryotes nature to the geological record. Proteins and few structurally preserved or morphologically nucleic acids have a low probability of preserva- distinctive microfossils. One of the few well- tion, but lipids can preserve well, and sterols in documented and widely accepted fossil occur- particular have been used to investigate the deep rences in earlier Archean rocks, and perhaps the history of eukaryotes. Abundant steranes (the only one that potentially bears on stem group geologically stable derivatives of sterols) extract- eukaryotes, comes from 3200-Mya shales that ed from petroleum document a Phanerozoic contain large (30–300 mm) spheroidal vesicles history of primary producers in the oceans (Javaux et al. 2010). These appear to be genuine that, to a first approximation, parallels the his- fossils, and they could, in principle, be eukary- tories inferred from microfossils and molecular otic; however, their simple ultrastructure and clocks (Knoll et al. 2007). Molecular fossils ex- ready comparison to the extracellular envelopes tend that record into Proterozoic and, more of some bacteria saps confidence from such an controversially, late Archean rocks. interpretation. Together then, phylogenies and preserva- In the absence of a convincing microfossil tion potential furnish guides to the paleobiolo- record, geobiologists have turned to molecular gy of early eukaryotic evolution, providing hy- fossils. Steranes of hypothesized eukaryotic or- potheses of evolutionary history. How well do igin have been reported from late Archean sedi- fossils fit these predictions? mentary rocks (Brocks et al. 1999; Waldbauer et al. 2009), potentially documenting early eu- karyotes, but raising incompletely resolved en- ARCHEAN EUKARYOTES? vironmental, phylogenetic, and geological is- The three-domain view of life, predicated on sues. The environmental concern is that sterol comparisons of SSU rRNA gene sequences, pos- biosynthesis requires molecular oxygen, yet ited that eukaryotes are sister
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