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TESTING the PROTOZOAN HYPOTHESIS for EDIACARAN FOSSILS: a DEVELOPMENTAL ANALYSIS of PALAEOPASCICHNUS by JONATHAN B

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TESTING the PROTOZOAN HYPOTHESIS for EDIACARAN FOSSILS: a DEVELOPMENTAL ANALYSIS of PALAEOPASCICHNUS by JONATHAN B [Palaeontology, Vol. 54, Part 5, 2011, pp. 1157–1175] TESTING THE PROTOZOAN HYPOTHESIS FOR EDIACARAN FOSSILS: A DEVELOPMENTAL ANALYSIS OF PALAEOPASCICHNUS by JONATHAN B. ANTCLIFFE1, ANDREW J. GOODAY2 and MARTIN D. BRASIER3 1Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS81RJ, UK; e-mail: [email protected] 2National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK; e-mail: [email protected] 3Department of Earth Sciences, Oxford University, South Parks Road, Oxford OX1 3AN, UK; e-mail: [email protected] Typescript received 21 October 2009; accepted in revised form 16 May 2011 Abstract: The hypothesis that the Ediacara biota were giant isms usually referred to the Ediacara biota, such as Charnia protozoans is tested by considering the external morphology, and Dickinsonia. Developmental analysis of the Palaeopascich- internal organization, suggested fossil representatives and nus – central to the xenophyophore hypothesis – reveals unu- molecular phylogeny of the xenophyophores. From this anal- sual, protozoan features, including evidence for chaotic repair ysis, we find no case to support a direct relationship. Rather, structures, for mergence of coeval forms, as well as complex the xenophyophores are here regarded as a group of recently bifurcations. These observations suggest that Palaeopascichnus evolved Foraminifera and are hence unlikely to have a record is a body fossil of an unidentified protozoan but is unrepre- from the Ediacaran Period. Further from the growth dynam- sentative of Ediacaran body construction, in general. ics of Foraminifera, they are also unlikely to be related to the Palaeopascichnus organism. We also find significant distinc- Key words: Palaeopascichnus, Ediacara biota, Protozoa, xeno- tions in the growth dynamics of Palaeopascichnus and organ- phyophores, development, evolution. The fossil record contains a great conundrum; the mod- 1994), who questioned the evidence for continuity ern animal phyla appear already distinguished as fossils between the Ediacara biota and succeeding Cambrian within the Cambrian System (Brasier 1979). This system metazoans. Seilacher (1989) also challenged the taxonomy lies immediately above the recently named Ediacaran Sys- by stating that many Ediacaran organisms share a com- tem (Knoll et al. 2004). From the time of Darwin to the mon construction. This was taken to imply that they are, discovery of the global Ediacara biota (Gu¨rich 1933; for the most part, a single clade unrelated to modern Sprigg 1947; Ford 1958), the ancestry of animals has groups. A profusion of taxonomic affinities has followed remained one of the most exciting mysteries in science. (e.g. Dzik 2003; Gehling 1991; Jenkins 1992; Valentine Indeed, Darwin (1859) stated that one of the greatest flaws 1992; Seilacher 2003; Seilacher et al. 2003; Peterson et al. in his hypothesis was the lack of demonstrable ancestry to 2003; Narbonne 2005). These taxonomies were based the recognized phyla that appear distinct at the base of the upon simple morphological, ecological and functional known fossil record (then ‘Silurian’, now the base of the comparisons. Latterly, this has been shown to be insuffi- Cambrian). After the great antiquity of the Ediacara biota cient as a rationale (see Antcliffe and Brasier 2008; Brasier had been realized (Ford 1958), then the Ediacara biota and Antcliffe 2009). was interpreted as primitive metazoans (Glaessner 1966, To date, there has been only one attempt at a cladistic 1984; Glaessner and Daily 1959; Glaessner and Wade analysis of the features of Ediacaran body fossils (Brasier 1966; Wade 1972; Jenkins 1984, 1985, 1992, 1995; Jenkins and Antcliffe 2009). Cladistic analysis arose from a con- and Gehling 1978; McMenamin 1986, 1998; Bengtson sideration of the flaws that can arise when relationships 2003), thereby providing putative solutions to the long are inferred from the use of functional analogues alone. posed problem regarding animal ancestry. Cladists argue that we must seek homologies instead (see This view of Ediacaran palaeobiology was refocused by Patterson 1982 for a complete discussion of the nature of Seilacher (1984, 1985, 1989, 1992; also Buss and Seilacher homology; see also De Beer 1971). It is clear from such ª The Palaeontological Association doi: 10.1111/j.1475-4983.2011.01058.x 1157 1158 PALAEONTOLOGY, VOLUME 54 methods that the establishment of relationships based not been demonstrated) to prove that they are related only on ecological and functional comparisons will be (i.e. both single-celled xenophyophores). These assump- ambiguous at best and misleading at worst. We have tions therefore entail the conclusions. That being so, then explored this question of homology at length elsewhere the potential xenophyophore affinities of the Ediacara (Brasier and Antcliffe 2004; Antcliffe and Brasier 2007b, biota appear to be questionable. Further, the basis for 2008), and we emphasize that for enigmatic fossils, such these assumptions can also be regarded as questionable. as the Ediacara biota, the most convincing route to estab- For example, there is now good evidence that many lish the hypotheses of biological affinity is likely to arise members of the frondose Ediacara biota (e.g. Charnia) from attempts to understand their developmental pro- lived at a great variety of water depths (Dalrymple and gramme. Narbonne 1996; Wood et al. 2003). Their abundance below the photic zone has therefore led Narbonne (1998, 2005) to dismiss the suggestion of McMenamin (1986, THE XENOPHYOPHORE HYPOTHESIS 1998) that such fronds housed photoautotrophic endo- symbionts in a manner similar to modern cnidarians. Seilacher et al. (2003), following the conception by Zhu- Further to this, all known xenophyophores currently inha- ravlev (1993), suggested that many members of the Edia- bit the deep sea (500–8000 m; Lemche et al. 1976), making cara biota could be regarded as relatives of an extant it highly unlikely that the architecture of their tests is con- group of amoeboid protozoans, the xenophyophores. The nected to housing photoautotrophic endosymbionts. latter group was established by Schulze (1906) and has The Ediacaran fossil Palaeopascichnus, found in Austra- been placed at different taxonomic levels from a family to lia, northern Norway, Avalonia (Newfoundland Canada, a phylum (Tendal 1996). Seilacher et al. (2003) suggested, Wales, Central England) and the Ukraine, has hitherto for the first time, that a protozoan organization is appro- been central to the xenophyophore hypothesis. Below, the priate for the Ediacara biota. It is important to note that morphology and development of this fossil is analysed these authors exempted the following Ediacaran organ- and contrasted with that of foraminiferan groups and, in isms from xenophyophore affinity: Kimberella, which is particular, with xenophyophores. Finally, we will examine regarded as ‘probably a mollusc’ (following Fedonkin and whether other members of the Ediacara biota were proto- Waggoner 1997), and Arkarua Gehling, seen sceptically zoan. as ‘a possible echinoderm’ (following Glaessner 1984; Gehling 1987). An affinity between the many remaining Ediacaran fos- DEVELOPMENTAL ANALYSIS OF sils and the xenophyophores was based on the following PALAEOPASCICHNUS line of reasoning, here summarized from the study by Seilacher et al. (2003). First, the external morphology of The fossil Palaeopascichnus Palij, 1976 was first described the xenophyophores closely resembles that of certain Edi- as an ichnofossil (Palij et al. 1979) from the Ediacaran acaran ‘trace fossil’ genera such as Yelovichus, Palaeopasc- (Vendian) of the Ukraine. Fedonkin (1978) considered ichnus, Neonerites and Intrites. Secondly, the Ediacara these specimens to represent the traces made by alternate biota shows structural features that are ‘similar’ to those right and left movements of an animal feeding appendage seen in the xenophyophores, argued to be adaptations for upon the bedding plane. Comparable, but poorly pre- unicellular gigantism. These adaptations include ‘similar- served material was discovered in Australia in the late ity in cell shape, subdivision of the cell and the nature of 1980s, but this was considered by Haines (1987 unpub- the fill skeletons.’ Finally, these authors inferred the pres- lished thesis, 1990) to represent algal body fossils rather ence of photoautotrophic endosymbionts, much as seen than animal traces. Haines (2000) later examined better in many extant larger benthic Foraminifera that divide a preserved material from Australia, inferring it to be of giant cell into compartments, to create smaller chamber- algal (possibly of phaeophyte) affinity based on simple lets for the housing of symbionts (e.g. Alveolina, Nummu- morphological comparisons with the extant calcareous lites and Fusulina; Armstrong and Brasier 2004). brown alga Padina. By this time, Jenkins (1995) had It is important to note here that xenophyophores are already argued that these Australian specimens were recognized and classified into families and genera partly meandering trace fossils of unknown affinity. Gehling on the basis of their internal organization, meaning their et al. (2000) dismissed this view because of taphonomic fossil record can be expected to be problematic. The features that were not, unfortunately, described. Jensen problem here is that Seilacher et al. (2003) have inferred (2003) analysed the material
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