Jonathan B. Antcliffe

Giving the early fossil record of sponges a squeeze.

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.

Charnia and sea pens are poles apart

Charnia from the Ediacara biota is here examined in terms of its growth and development. The Ediacara biota comes from the critical period of evolution just before the Cambrian Explosion and is key to our understanding of the origin of animal life. We show that Charnia cannot be related to the modern cnidarian group the sea pens (Pennatulacea) with which it has for so long been compared, as generative zones cannot be homologized between these forms.

Changing the picture of Earth's earliest fossils (3.5-1.9 Ga) with new approaches and new discoveries.

Significance Precambrian fossils are essential for understanding the emergence of complex life. New analytical tools and new fossil discoveries are now changing the picture, allowing us to refine and extend our knowledge about the early fossil record. High-resolution data from 3.46-Ga Apex chert microbiota help us to test rigorous criteria for studying the early fossil record. Preservational windows in the 1.88-Ga Gunflint chert allow us to posit novel cellular forms, and emphasize the critical role played by the fossil record in understanding early biodiversity. Micromapping of 3.43-Ga Strelley Pool sandstone reveals microfossils preserved between sand grains from the earliest known shoreline, reminding us that many kinds of ancient habitat have yet to be explored in this way. New analytical approaches and discoveries are demanding fresh thinking about the early fossil record. The 1.88-Ga Gunflint chert provides an important benchmark for the analysis of early fossil preservation. High-resolution analysis of Gunflintia shows that microtaphonomy can help to resolve long-standing paleobiological questions. Novel 3D nanoscale reconstructions of the most ancient complex fossil Eosphaera reveal features hitherto unmatched in any crown-group microbe. While Eosphaera may preserve a symbiotic consortium, a stronger conclusion is that multicellular morphospace was differently occupied in the Paleoproterozoic. The 3.46-Ga Apex chert provides a test bed for claims of biogenicity of cell-like structures. Mapping plus focused ion beam milling combined with transmission electron microscopy data demonstrate that microfossil-like taxa, including species of Archaeoscillatoriopsis and Primaevifilum, are pseudofossils formed from vermiform phyllosilicate grains during hydrothermal alteration events. The 3.43-Ga Strelley Pool Formation shows that plausible early fossil candidates are turning up in unexpected environmental settings. Our data reveal how cellular clusters of unexpectedly large coccoids and tubular sheath-like envelopes were trapped between sand grains and entombed within coatings of dripstone beach-rock silica cement. These fossils come from Earth’s earliest known intertidal to supratidal shoreline deposit, accumulated under aerated but oxygen poor conditions.

Early life: Origins of multicellularity

Interpreting truly ancient fossils is an especially tricky business. The conclusion that 2.1-billion-year-old structures from Gabon are the remains of large colonial organisms will get palaeobiologists talking.

The oldest evidence of bioturbation on Earth: COMMENT

Here we question the conclusions of Rogov et al. (2012), who claim to describe “the oldest evidence of bioturbation on Earth” in the form of meniscate backfi lled burrows and escape traces from late Ediacaran car- bonates of the Siberian Khatyspyt Formation. Because trace fossils can constrain early Metazoan origins, and are used to defi ne the base of the Cambrian Period (Brasier et al., 1994), such a signifi cant claim requires jus- tifi cation by careful interpretation of the material, and critical analysis, both of which appear wanting here. Although we agree that multiple biological and ecological revolutions took place during the late Ediacaran Period, we question whether those events can be tied to these problematic fossils.

Evolutionary Trends in Remarkable Fossil Preservation Across the Ediacaran–Cambrian Transition and the Impact of Metazoan Mixing

A unifying model is presented that explains most of the major changes seen in fossil preservation and redox conditions across the Precambrian–Cambrian transition. It is proposed that the quality of cellular and tissue preservation in Proterozoic and Cambrian sediments is much higher than it is in more recent marine deposits. Remarkable preservation of cells and soft tissues occurs in Neoproterozoic to Cambrian cherts, phosphates, black shales, siliciclastic sediments and carbonates across a wide range of environmental conditions. The conditions for remarkable preservation were progressively restricted to more marginal environments through time, such as those now found in stagnant lakes or beneath upwelling zones. These paradoxes can no longer be adequately explained by recourse to a series of ad hoc explanations, such as those involving unusually tough organic matter in the Ediacaran, or unusual seawater chemistry, or even the role of microbial biofilms alone. That is because the exceptions to these are now too many. Instead, we suggest that elevated pore water ion concentrations, coupled with the almost complete lack of infaunal bioturbation, and hence the lack of a sediment Mixed-layer, provided an ideal environment for microbially-mediated ionic concentrations at or near the sediment–water interface. These strong ionic gradients encouraged early cementation and lithification of sediments, often prior to complete decomposition of delicate organic structures. Seen in this way, not only did the biosphere evolve across the Precambrian–Cambrian transition. Fossilization itself has evolved through time, and never more dramatically so than across this interval.

Critical questions about early character acquisition-comment on Retallack 2012 : "some Ediacaran fossils lived on land".

The Ediacaran Period (ca. 635–541 Ma) and the enigmatic fossil biota it contains are the cause some of the most vigorous debate in paleontology. Some argue the Ediacaran biota represents animal ancestors (Gehling 1991; Erwin et al. 2011) while others contend otherwise (Budd and Jensen 2000; Antcliffe and Brasier 2007). There are considerable debates about the taxonomy (Laflamme and Narbonne 2008; Brasier et al. 2010), and to what degree differences between the fossils and fossil sites are taphonomic (Liu et al. 2011; Gehling and Droser 2013), evolutionary (Gehling 1991), ontogenetic (Brasier and Antcliffe 2004), or environmental (Grazhdankin 2004; Gehling and Droser 2013). Many phylogenetic hypotheses have been considered for Ediacaran fossils (see Fig. 1): animal groups (Gehling 1991), fungi (Peterson et al. 2003), foraminifera (Seilacher et al. 2003), photosynthetic algae (Ford 1958), lichens (Retallack 1994), or even lost kingdoms of unknown affinity (Seilacher 1992). One way to test these phylogenetic hypotheses is to examine the environments in which the organisms lived, and much recent work has rightly had this focus (e.g. Gehling 2000; Gehling and Droser 2013). The strata from Canada and the UK are demonstrably deep marine (Benus 1988) and share taxa with Australian and Russian localities. This means the Ediacaran biota (e.g., Charnia) cannot be photosynthetic algae, as they demonstrably lived too deep in the ocean to photosynthesize. In a similar way, we are able to reject the idea that the Ediacaran fossils represent terrestrial lichens (Retallack 1994, 2012), because there is no convincing evidence that the strata were terrestrial and there is conclusive evidence that they were marine, and some were deep marine (Callow et al. 2012). This historical link in Ediacaran paleobiology between environmental interpretation and possible phylogenetic affinities helps us to understand why Retallack (2012) is concerned with demonstrating a permissive environment for the lichen hypothesis of Retallack (1994). However, while environment can rule out hypotheses of biological affinities it cannot confirm a hypothesis as true. Even if we grant Retallack (2012) his environmental interpretation it does not mean the Ediacaran biota were lichens because lichens are not the only organisms capable of living on land. The original arguments for a lichen affinity in Retallack (1994) were based on the idea that Dickinsonia’s body was woody and tough not soft and gelatinous. This idea was coherently disputed by Waggoner (1995) and later disproven by detailed taphonomic study (Brasier and Antcliffe 2008). When examining enigmatic fossils we must understand what diagnostic characters are present that allow us to confidently place these fossils with their closest living relatives.What are the characters present in Ediacaran organisms that lead logically to the conclusion that these organisms are the remains of ancient lichens? How was it determined that such characters are unique to lichens to the exclusion of other similar morphological shapes or structures formed by abiological processes? The answers to these questions are not forthcoming. This means there is no evidence to support the biological claims of Retallack (2012), which seems to rely on correlative confirmation bias to a highly contentious interpretation of a terrestrial environment. In one thing alone, however, Retallack (2012) is right: in general we should not assume that macroscopic size implies animal affinities for enigmatic fossils. Almost all of the major eukaryotic lineages shown in Figure 1 have members with the ability to achieve macroscopic size. This is because, like with lichens, coloniality and symbiotic associations allow unicells to outgrow their microscopic origins. The possible affinities of the Ediacaran biota have hitherto been too opisthokont focused and we should widen our search to the rest of the macroscopic marine Eukarya. In the meantime, we should not be distracted by false debates about terrestrial sediments.

Towards a morphospace for the Ediacara biota

Abstract The Ediacara biota of the late Neoproterozoic is justly famous as a biological puzzle. Studies of Ediacaran biology have commonly used analogy with living organisms as a cipher for the decoding of biological affinity, and consequently the life mode and habit. Here, we discuss the problems of using such analogous reasoning and put forward our alternative approach, that of using Morphospace Analysis for the study of growth, form and phylogeny. This tool, we suggest, has the potential to be used for testing the unity of an evolutionary clade, such as ‘rangeomorphs’ and ‘dickinsoniomorphs’. Preliminary data from the members of the Ediacara biota do indeed show such a unity within our preliminary morphospace model (all k values are low). This method reveals no clear relationships, between these forms and more recent biological groups such as the sea pens or the Foraminifera.

Reply to Retallack (2013): Ediacaran characters

How should we use characters to place fossil organisms with their closest living relatives? The last 40 years have favored a solution that uses plesiomorphic and apomorphic characters and the cladistic methodology. This can be difficult for fossil taxa as the characters that define groups must be unique and present in the group’s last common ancestor, and agreeing what these are can be a challenge. Nonetheless, the cladistic approach has had great success in unravelling the evolutionary relationships and affinities of other enigmatic fossils, such as those of the Burgess Shale. However, Retallack (2013a, 2013b) instead argues for a phenetic approach that identifies affinity based on overall similarity, and his conclusions are erroneous as a result. Retallack (2013b) indeed seems to be aware of this problem referring to phenetics as “picture matching” and stating that he is not engaged in such a process. However, below we demonstrate how Retallack (2013b) does use a phenetic approach and how this has led him to misunderstand the criticisms of Antcliffe and Hancy (2013) and restate all the same errors. None of the characters listed in Retallack (2013b) or his previous publications convincingly identify any Ediacaran fossils (c. 575–545Ma ago) as lichens. To demonstrate a logical connection between an enigmatic fossil and a lichen, that fossil must have characters unique to lichens. This must be presented in such a way that other scientists can verify that the characters are present in the fossil, and if real are not the result of a preservational artefact or some other abiological process. In attempting to answer this challenge Retallack (2013b) lists eighteen characters allegedly present in the iconic Ediacaran fossil Dickinsonia. The anatomy of Dickinsonia has been extensively studied (e.g., Brasier and Antcliffe, 2008) and the vast majority of characters listed in Retallack (2007, 2013b) have not been recognized as real and/or significant by any other scientist. Retallack (2013b) argues these characters collectively add up to making the lichen hypothesis so much more likely than several other hypotheses that it should form the basis of a null hypothesis for Ediacaran fossils that are “best considered fundamentally fungal until proven otherwise” (Retallack, 2013b). Attempting to shift the burden of proof must always be challenged head on. Clearly the most reasonable null hypothesis for any group of enigmatic fossils is that “the fossils are of unknown affinity.” The Retallack (2013b) argument is based on percentile similarity, not evolutionary history and character acquisition. Retallack (2013b) states “characters are tabulated for comparison with alternative biological affinities by Retallack (2007, Table 5), with the result that lichens and non‐lichenized fungus fully (100%) explain 16 characters ofDickinsonia, but only 81% are explained by xenophyophores and cnidarian polyps.” If 100% of characters are possessed by lichen and non‐lichen fungi and 81% by xenophyophores (a group of giant foraminifera see Antcliffe et al. 2011) and by cnidarian polyps, then only 19% of these characters are of any use. The 81% of characters shared by these groups are useless for making higher taxonomic distinctions. The three characters not possessed by xenophyophores and cnidarians (5, 7, and 12; see Table 1 below) are described with language loaded towards a fungal interpretation (thallus, hypothallial rims, and rhizine) but which could easily be applied to these taxa if they were given less leading character names (i.e., undifferentiated tissue, rims around edge of circular fossils, and filamentous, respectively). Why are these simple characters best described as “thallus” or “hypothallial” or “rhizine,” which imply affinity, rather than by more generic description‐based alternatives? That is precisely the question that has not been answered by Retallack (2007, 2013a, 2013b). The “rhizine” filaments are not even characters of Dickinsonia, but are part of the microbial filaments that cover Ediacaran age bedding planes even when macrofossils are not present. What of the remaining characters (see Table 1 below)? Five (characters 14–18) pertain to environmental context of the fossil and are not characters of the fossil themselves (e.g., can live on land or on top of microbial mats), one (character 10) is a biomechanical interpretation and not a diagnostic character, and at least five other characters (characters 1, 2, 9, 11, and 13) are meaningless as applied to these fossils (e.g., describing the fossils as “fractal” is only colloquial). Finally, many “characters” lack robust statistical support (e.g., “isometric growth in width and length” (character 3), “avoidance of other individuals” (characters 4, 6 and 8), but even if true they have no phylogenetic significance because they are found amongst very many other groups of organisms. No unique and real characters have been identified, and all of the characters listed could, for example, also be found in cnidarians or foraminifera. Taking a slightly wider view than just the Dickinsonia example discussed by Retallack (2013b) it similarly becomes clear that no distinctive lichen characters have ever been convincingly demonstrated for any Ediacaran age fossil. EVOLUTION & DEVELOPMENT 15:6, 389–392 (2013)

Distinguishing Earth’s oldest known bryozoan (Pywackia, late Cambrian) from pennatulacean octocorals (Mesozoic–Recent)

Abstract. Bryozoans and all biomineralized metazoan phyla extend back into the Cambrian. Pywackia Landing, 2010 is confirmed as a secondarily phosphatized, late Cambrian stenolaemate bryozoan with colonial habit; mineralized zooarium (originally calcareous); granular/rarely granular-prismatic histology of its trilamellar walls; and polymorphism shown by deep autozooecia with diaphragms and hemiphragms, axial zooecia with diaphragms, and probable nanozooecia. The irregular form of Pywackia reflects growth as a 14-hedron that could not branch and a lack of structures such as thickened walls or styles that maintain regular autozooecial spacing in later stenolaemates. Pywackia is a stem group stenolaemate with a stolon modified into a budding axial zooid and autozooid budding. It is morphologically simpler than the highly evolved late Tremadocian bryozoans of South China with features such as styles, cystiphragms, thickened zooecial walls, and massive or branching colonies. As with some bryozoans, Pywackia lacks holdfasts but has lineated living chambers and variably sized autozooecia. The late Cambrian origin of bryozoans, euconodonts, polyplacophorans, and cephalopods set the stage for the Ordovician Radiations complex communities. Pywackia is not a pennatulacean octocoral. It lacks both a pennatulacean axial rod histology and a budding zooid that remains confluent with daughter autozooids. Indeed, Pywackia walled off its axial zooid. Similarity of the 6- and 12-sided Pywackia zooarium with circular to 4-sided pennatulacean axes only includes calcareous composition and the general shapes of Pywackia zooaria and some Lituaria axial rods. The pennatulacean record does not extend from the Mesozoic into the Cambrian, and early cnidarians were not phosphatic. The diagnosis of Pywackia is modified.