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Giving the Early Fossil Record of Sponges a Squeeze

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Biol. Rev. (2014), pp. 000–000. 1 doi: 10.1111/brv.12090 Giving the early fossil record of sponges a squeeze Jonathan B. Antcliffe1,2,∗,RichardH.T.Callow3 and Martin D. Brasier4,5 1Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, U.K. 2Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS81RJ, U.K. 3Department of Geology and Petroleum Geology, School of Geosciences, University of Aberdeen, Meston Building, Aberdeen AB24 3UE, U.K. 4Department of Earth Sciences, Oxford University, Parks Road, Oxford OX13PR, U.K. 5Department of Earth Sciences, Memorial University of Newfoundland, 300 Prince Philip Drive, St John’s A1B 3X5, Canada ABSTRACT Twenty candidate fossils with claim to be the oldest representative of the Phylum Porifera have been re-analysed. Three criteria are used to assess each candidate: (i) the diagnostic criteria needed to categorize sponges in the fossil record; (ii) the presence, or absence, of such diagnostic features in the putative poriferan fossils; and (iii) the age constraints for the candidate fossils. All three criteria are critical to the correct interpretation of any fossil and its placement within an evolutionary context. Our analysis shows that no Precambrian fossil candidate yet satisfies all three of these criteria to be a reliable sponge fossil. The oldest widely accepted candidate, Mongolian silica hexacts from c. 545 million years ago (Ma), are here shown to be cruciform arsenopyrite crystals. The oldest reliable sponge remains are siliceous spicules from the basal Cambrian (Protohertzina anabarica Zone) Soltanieh Formation, Iran, which are described and analysed here in detail for the first time. Extensive archaeocyathan sponge reefs emerge and radiate as late as the middle of the Fortunian Stage of the Cambrian and demonstrate a gradual assembly of their skeletal structure through this time coincident with the evolution of other metazoan groups. Since the Porifera are basal in the Metazoa, their presence within the late Proterozoic has been widely anticipated. Molecular clock calibration for the earliest Porifera and Metazoa should now be based on the Iranian hexactinellid material dated to c. 535 Ma. The earliest convincing fossil sponge remains appeared at around the time of the Precambrian-Cambrian boundary, associated with the great radiation events of that interval. Key words: Precambrian, Porifera, fossil calibration, sponges, Ediacaran, origin of animals, macroevolution, Cambrian explosion. CONTENTS I. The Cambrian explosion ................................................................................... 2 II. The phylogeny of animals and the characteristics of Porifera ............................................... 2 (1) Potentially useful characteristics of hexactinellids and demosponges ................................... 4 (2) Potentially useful characteristics of calcareous sponges ................................................. 4 III. Case studies from the Cambrian: Archaeocyatha and stem group sponges ................................. 5 IV. The earliest poriferan candidates ........................................................................... 8 (1) An organic walled vesicle, Wynniatt Formation, Canada (between 723 and 1077 Ma) ................ 9 (2) Jacutianema and related forms, Lakhanda Sequence, Russia, c. 1020 Ma .............................. 10 (3) Otavia antiqua, a ‘sponge-like’ fossil from Namibia c. 760 Ma ........................................... 11 (4) ‘Sponge spicules’ from Nevada, USA c. 750 Ma ....................................................... 11 (5) Organic ‘demosponge biomarkers’ from the Cryogenian of Oman .................................... 11 (6) ‘Pre-Varangerian’ monaxons from Alaska and northwest Canada ..................................... 13 (7) ‘Pre-Marinoan bioclasts’, South Australia .............................................................. 13 (8) Monaxons and body fossils from Doushantuo Formation, China ...................................... 13 (9) Thectardis avalonensis from Newfoundland c. 565–555 Ma .............................................. 14 * Address for correspondence (E-mail: [email protected]). Biological Reviews (2014) 000–000 © 2014 The Authors. Biological Reviews © 2014 Cambridge Philosophical Society 2 Jonathan B. Antcliffe and others (10) Fedomia mikhaili from Russia c. 558–555 Ma ........................................................... 14 (11) Ausia from Namibia c. 555 Ma ......................................................................... 15 (12) Vaveliksia vana from Russia c. 555 Ma ................................................................... 16 (13) Palaeophragmodictya from Australia c. 555 Ma ........................................................... 16 (14) Cucullus fraudulentus from the Miaohe Biota, China c. 555 Ma .......................................... 17 (15) Spicules from the Doushantuo and Dengying Formations, China, c. 550 Ma .......................... 17 (16) Namapoikia, Namacalathus and spicules from Namibia c. 549 Ma ........................................ 17 (17) Hexaxon spicules from Mongolia c. 545 Ma ........................................................... 18 (18) Spicules from the Lower Tal Formation, Lesser Himalaya, India ...................................... 18 (19) Spicules from the Soltanieh Formation, Northern Iran c. 535 Ma ..................................... 21 (20) Fossils from various localities in Siberia, Lower Cambrian ............................................. 23 V. A discussion of our search criteria for the earliest sponge fossils ............................................ 24 VI. A discussion constraining the origin of sponges ............................................................. 25 VII. Conclusions ................................................................................................ 29 VIII. Acknowledgements ......................................................................................... 29 IX. References .................................................................................................. 29 I. THE CAMBRIAN EXPLOSION (Seilacher, 1977; Bottjer et al., 2000; Orr, Benton & Briggs, 2003). The Precambrian-Cambrian boundary is a fundamental These many lines of evidence suggest that animal groups dividing line in the history of life. This boundary separates emerged near the base of the Cambrian Period and an earlier world with no certain animal remains, lasting for quickly established ecological feedbacks resulting in the some 4000 million years, from a later world where undoubted construction of these first complex ecosystems (Butterfield, animal remains abound. The fossil record indicates that 2007). Precambrian fossils, however, including candidate all the major animal phyla appeared in an interval of animals, have been much more difficult to interpret. Finding approximately 30 million years following the Ediacaran- definitive Precambrian crown-group animal characteristics Cambrian boundary. However, Precambrian ancestors is the only way to refute a relatively late radiation of animals. to the Metazoa have long been sought (e.g. Glaessner, In practice this is complicated by the lack of generally agreed 1984; Gehling, 1991; Runnegar & Fedonkin, 1992; criteria for what such organisms might look like, or how Fedonkin & Waggoner, 1997; Sperling, Pisani, & Peterson, we might otherwise recognize them. This is particularly 2007). important for sponges, both as animals that might have a The Cambrian fossil record of animals contains a low preservation potential, and because they are generally coherent and well-documented set of evidence. This includes recovered as being basal or a sister group to all other animals. evidence for: the origin of bioturbation (Cowie & Brasier, Our aim is thus to erect criteria and establish a methodology 1989; McIlroy & Logan, 1999); the first direct evidence for assessing such (generally controversial) claims. In turn of zooplankton (e.g. the phosphatocopid Klausmuelleria this allows us to address a series of exciting questions, such salopiensis from the Lower Cambrian Comley Limestone; as: did deep ancestors have negligible fossilization potential see Hinz, 1987; Siveter, Williams, & Waloszek, 2001; or has the fossil record of early animal evolution been Siveter, Waloszek, & Williams, 2003; Harvey, Velez,´ & misinterpreted? Does our approach to classifying fossil taxa inevitably lead us to assign them to relatively derived, rather Butterfield, 2012); the rapid expansion of biomineralisation than more basal positions? Or have fossil problematica, (Porter, 2007, 2010; Brasier, Antcliffe & Callow, 2011); such as the Ediacaran biota, been incorrectly assigned to the construction of the first animal reef systems (Gandin plesiomorphic positions within metazoan phylogeny? & Debrenne, 2010); the assembly of solid exoskeletons from multiple skeletal elements (e.g. Bengtson, 1985, 1992; Bengtson et al., 1990); the diachronous geographical spread of new metazoan groups (Cowie & Brasier, 1989); and II. THE PHYLOGENY OF ANIMALS AND THE the continued radiation of these new groups (Marshall, CHARACTERISTICS OF PORIFERA 2006). Changes in ocean chemistry also appear to have followed the emergence of early animal activity, including Sponges are positioned near the base of the animal a reduction of oceanic dissolved organic carbon owing group (Halanych, 2004; Srivastava et al., 2010) and so to zooplankton ventilaton
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  • Palaeobiology and Diversification of Proterozoic-Cambrian Photosynthetic Eukaryotes

    Palaeobiology and Diversification of Proterozoic-Cambrian Photosynthetic Eukaryotes

    Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1308 Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-554-9389-9 UPPSALA urn:nbn:se:uu:diva-265229 2015 Dissertation presented at Uppsala University to be publicly examined in Hambergsalen, Geocentrum, Villavägen 16, 752 36, Uppsala, Friday, 11 December 2015 at 10:15 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Professor Shuhai Xiao (Geosciences, Virginia Polytechnic Institute and State University). Abstract Agić, H. 2015. Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1308. 47 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-554-9389-9. One of the most important events in the history of life is the evolution of the complex, eukaryotic cell. The eukaryotes are complex organisms with membrane-bound intracellular structures, and they include a variety of both single-celled and multicellular organisms: plants, animals, fungi and various protists. The evolutionary origin of this group may be studied by direct evidence of past life: fossils. The oldest traces of eukaryotes have appeared by 2.4 billion years ago (Ga), and have additionally diversified in the period around 1.8 Ga. The Mesoproterozoic Era (1.6-1 Ga) is characterised by the first evidence of the appearance complex unicellular microfossils, as well as innovative morphologies, and the evolution of sexual reproduction and multicellularity. For a better understanding of the early eukaryotic evolution and diversification patterns, a part of this thesis has focused on the microfossil records from various time periods and geographic locations.