The Beothukis/Culmofrons problem and its bearing on Ediacaran macrofossil taxonomy: evidence from an exceptional new fossil locality

The late Ediacaran siliciclastic successions of eastern Newfoundland, Canada, are renowned for their fossils of soft‐bodied macro‐organisms, which may include some of the earliest animals. Despite the potential importance of such fossils for evolutionary understanding, the taxonomic framework within which Ediacaran macrofossils are described is not clearly defined. Rangeomorphs from a newly discovered fossil surface on the Bonavista Peninsula, Newfoundland, require us to reconsider contemporary use of morphological characters to distinguish between genera and species within Ediacaran taxa. The new surface exhibits remarkable preservational fidelity, resolving features smaller than 0.1 mm in dimension in both frondose and non‐frondose taxa. Such preservation permits the recognition of rarely observed fourth‐ and fifth‐order rangeomorph branching, offering unparalleled opportunities to investigate the fine‐scale construction of rangeomorph taxa including Culmofrons plumosa Laflamme et al., 2012. Our observations enable resolution of taxonomic issues relating to rangeomorphs, specifically overlap between the diagnoses of the frondose genera Beothukis Brasier and Antcliffe, 2009 and Culmofrons. We propose a taxonomic framework for all Ediacaran macrofossils whereby gross architecture, the presence/absence of discrete morphological characters and consideration of growth programme are used to distinguish genera, whereas morphometric or continuous characters define taxa at the species level. On the basis of its morphological characters, Culmofrons plumosa is herein synonymized to a species (Beothukis plumosa comb. nov.) within the genus Beothukis. This discussion emphasizes the need to standardize the taxonomic approach used to describe Ediacaran macrofossil taxa at both the genus and species levels, and raises important considerations for future formulation of higher‐level taxonomic groups.     

Rangeomorphs,Thectardis (Porifera?) and dissolved organic carbon in the Ediacaran oceans

The mid-Ediacaran Mistaken Point biota of Newfoundland represents the first morphologically complex organisms in the fossil record. At the classic Mistaken Point localities the biota is dominated by the enigmatic group of "fractally" branching organisms called rangeomorphs. One of the few exceptions to the rangeomorph body plan is the fossil Thectardis avalonensis, which has been reconstructed as an upright, open cone with its apex in the sediment. No biological affinity has been suggested for this fossil, but here we show that its body plan is consistent with the hydrodynamics of the sponge water-canal system. Further, given the habitat of Thectardis beneath the photic zone, and the apparent absence of an archenteron, movement, or a fractally designed body plan, we suggest that it is a sponge. The recognition of sponges in the Mistaken Point biota provides some of the earliest body fossil evidence for this group, which must have ranged through the Ediacaran based on biomarkers, molecular clocks, and their position on the metazoan tree of life, in spite of their sparse macroscopic fossil record. Should our interpretation be correct, it would imply that the paleoecology of the Mistaken Point biota was dominated by sponges and rangeomorphs, organisms that are either known or hypothesized to feed in large part on dissolved organic carbon (DOC). The biology of these two clades gives insight into the structure of the Ediacaran ocean, and indicates that a non-uniformitarian mechanism delivered labile DOC to the Mistaken Point seafloor.     

A fungal analog for newfoundland ediacaran fossils?

We propose that some of the more conspicuous Ediacaran fossilsfrom the Avalon Peninsula of Newfoundland, including Aspidella,Charnia, and Charniodiscus, were biologically similar to membersof the Kingdom Fungi. These organisms were multicellular ormultinuclear, lived below the photic zone, could not move ordefoul themselves, did not exhibit taphonomic shrinkage, andwere not transported or moved. Aspidella, in particular, appearsto exhibit indeterminate growth without a maximum size constraint,and appears to show growth zonations similar to modern mycelia.Other fossils from this deposit exhibit a fractal-like growthpattern. Together, these features falsify algal, lichen, andmetazoan interpretations of these fossils, yet reflect characteristicsof modern fungal mycelia. We emphasize that although no MistakenPoint fossil appears to be a metazoan, not all of the MistakenPoint taxa, and not all of the Ediacaran organisms in general,can reasonably be interpreted using a fungal analogy. Furthermore,the hypothesis that these fossils were functionally fungus-likeneed not imply that the organisms were members of the crown-groupFungi. We propose further tests for evaluating both this functionalhypothesis and the phylogenetic hypothesis that these organismswere members of the total-group Fungi.     

Slime travelers: Early evidence of animal mobility and feeding in an organic mat world

Mobility represents a key innovation in the evolution of complex animal life. The ability to move allows for the exploration of new food sources, escapes from unfavorable environmental conditions, enhanced ability to exchange genetic material, and is one of the major reasons for the diversity and success of animal life today. The oldest widely accepted trace fossils of animal mobility are found in Ediacaran‐aged rocks (635–539 Ma). The earliest definitive evidence for movement associated with exploitation of resources for feeding occurs in the White Sea assemblage of the Ediacara Biota—macroscopic, soft‐bodied fossils of Ediacaran age. Here, we evaluate potential support for mobility in dickinsoniomorphs, presenting new data regarding abundant Dickinsonia and associated trace fossils from the Ediacara Member, South Australia. Results quantitatively demonstrate that Dickinsonia was capable of mobility on relatively short, ecological timescales. This organism was bilaterally symmetrical, likely moved via muscular peristalsis, and left trace fossils due to active removal of the organic mat related to feeding. Analogous structures associated with Yorgia indicate that it was also mobile and fed in a similar manner. Morphological evidence suggests that two other modular taxa, Andiva and Spriggina, were able to move but did not feed in a manner that impacted the organic mat. Together, these data suggest that mobility was present in multiple disparate bilaterally symmetrical Ediacaran taxa.     

A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes

SUMMARY Dickinsonia is one of the most recognizable forms in the Ediacaran fauna, but its phylogenetic position has been contentious, and it has been placed in almost every kingdom of life. Here, it is hypothesized that the affinities of Dickinsonia lie with the Placozoa (Metazoa), an understudied phylum that is widespread in tropical seas worldwide. Modern placozoans show obvious differences in size and axial organization compared with Dickinsonia, but these differences can be accounted for by the stem‐group/crown‐group distinction. The affinity with placozoans is evidenced primarily by the unique feeding mode of Dickinsonia, which is demonstrated by a series of feeding traces. These traces indicate that Dickinsonia moved over the Ediacaran matgrounds, and digested the mat using its entire lower sole. The ability of Dickinsonia to move negates an algal, fungal, or sponge affinity, while the feeding mode, external digestion with a ventral sole, rules out placement within any sponge or eumetazoan lineage. The only organisms that both move and feed in this manner are placozoans. Recent molecular phylogenetic studies have demonstrated that placozoans lie above sponges but below Eumetazoa. We hypothesize that Dickinsonia and other externally digesting Ediacaran forms are either stem‐placozoans, or a series of extinct lineages above sponges and below eumetazoans on the metazoan tree. We discuss the potential evolutionary transitions between the main metazoan feeding modes in the context of the emerging molecular phylogeny, and suggest that aspects of the sponge and placozoan feeding strategies are relicts of nonuniformitarian Proterozoic ocean conditions.     

Effaced preservation in the Ediacara biota and its implications for the early macrofossil record

Abstract: Ediacaran structures known as ‘pizza discs’ or Ivesheadia have long been considered enigmatic. They are amongst the oldest known members of the Ediacara biota, apparently restricted to the Avalonian successions of Newfoundland and the UK, c. 579–560 Ma. Here, we suggest that these impressions are taphomorphs, resulting from the post‐mortem decay of the frondose Ediacaran biota. Ediacaran fossils range from well‐preserved, high‐fidelity variants to almost completely effaced specimens. The effaced specimens are inferred to have undergone modification of their original morphology by post‐mortem microbial decay on the sea floor, combined with sediment trapping and binding. In this style of preservation, morphological details within the organism became variously subdued as a function of the extent of organic decay prior to casting by overlying sediments. Decay and effacement were progressive in nature, producing a continuum of grades of preservation on Ediacaran bedding planes. Fossils preserved by such ‘effaced preservation’ are those that have suffered these processes to the extent that only their gross form can be determined. We suggest that the lack of detailed morphology in effaced specimens renders such fossils unsuitable for use as type material, as it is possible that several taxa may, upon degradation and burial, generate similar morphological taphomorphs. We here reinterpret the genus Ivesheadia as a taphomorph resulting from extensive post‐mortem decay of frondose organisms. Blackbrookia, Pseudovendia and Shepshedia from beds of comparable age in England are likewise regarded as taphomorphs broadly related to Charnia or Charniodiscus spp. To reflect the suggestion that such impressions are likely to be taphomorphs, and not taxonomically discrete, we propose the term ivesheadiomorphs to incorporate all such effaced taphonomic expressions of Ediacaran macrofossil taxa in Avalonian assemblages. Our recognition of effaced preservation has significant implications for Ediacaran taxonomy, and consequently for measures of Ediacaran diversity and disparity. It is implied that Avalonian assemblages preserve both organisms that were alive and organisms that were already dead at the time of burial. As such, the fossil assemblages cannot be taken to represent census populations of living organisms, as in prior interpretations.     

Precambrian–Cambrian boundary interval occurrence and form of the enigmatic tubular body fossil Shaanxilithes ningqiangensis from the Lesser Himalaya of India

The affinity of the Ediacaran fossil Shaanxilithes ningqiangensis and putatively related forms has long been enigmatic; over the past few decades, interpretations ranging from trace fossils to algae to metazoans of uncertain phylogenetic placement have been proposed. Combined morphological and geochemical evidence from a new occurrence of S. ningqiangensis in the Krol and Tal groups of the Lesser Himalaya of India indicates that S. ningqiangensis is not a trace fossil, but rather an organic‐walled tubular body fossil of unknown taxonomic affinity. Specimens consist of compressed organic cylindrical structures, characterized by extended, overlapping or fragmented iterated units. Where specimens intersect, overlapping rather than branching or intraplanar crossing is observed. Lithologic comparisons and sequence stratigraphic data all suggest a late Ediacaran age for the uppermost Krol Group and basalmost Tal Group. By extending the biogeographical distribution of S. ningqiangensis, hitherto confined to the Ediacaran of China and potentially Siberia, to the Precambrian–Cambrian boundary interval of India, this new occurrence of S. ningqiangensis expands the biostratigraphic utility of this enigmatic fossil to the inter‐regional and intercontinental scale. Moreover, study of these new and exceptionally preserved samples may help to significantly constrain the long‐debated problem of Shaanxilithes' affinity, elucidating its ‘problematic’ status and shedding new light upon the ecology and taphonomy of one of the most significant intervals in early life history.     

The Ediacaran Aspidella‐type impressions in the Jinxian successions of Liaoning Province,northeastern China

Macroscopic impression fossils from the Xingmincun Formation of the Jinxian Group, Liaoning Province of northeastern China, are identified as members of the Aspidella plexus of Ediacaran age. This is the first recognition of the taxon in the Liaoning Province, although such fossils have been previously recorded in the succession, but were referred to as new species and relegated to an earlier Neoproterozoic age. A revision of the taxonomic interpretation and relative age estimation of the previous record is provided, as well as an evaluation of abiotic vs. biotic processes that could produce similar structures to studied impressions. The mode of preservation of the fossils is considered from a biochemical point of view and along with the properties of organic matter in the integument of soft‐bodied metazoans. The selective preservation of the Ediacaran organisms, including metazoans, as impressions (moulds and casts) against the organically preserved contemporaneous cyanobacterial and algal microfossils, and an exceptionally small number of terminal Ediacaran metazoan fossils (Sabellidites, Conotubus and Shaanxilithes), demonstrates the non‐resistant characteristics and the very different biochemical constitution of the Ediacaran metazoans compared with those that evolved in the Cambrian and after. The refractory biomacromolecules in cell walls of photosynthesizing microbiota (bacterans, cutans, algaenan and sporopollenin groups) and in the chitinous body walls of Sabellidites contrast sharply with the labile biopolymers in Ediacaran metazoans known only from impressions. The newly emerging biosynthesis of resistant biopolymers in metazoans (chitin and collagen groups) initiated by the annelids at the end of Ediacaran and fully evolved in Cambrian metazoans, considered with the ability to biomineralize, made their body preservation possible. The Chengjiang and Burgess Shale metazoans show evidence of this new biochemistry in body walls and cuticles, and not only because of the specific taphonomic window that enhanced their preservation.     

Diversification of the Metazoa: Ediacarans,colonies, and the origin of eumetazoan complexity by nested modularity

The Ediacaran biota is profoundly mysterious. There is a growing realization that these organisms should not be grouped in a single taxon, such as Petalonamae or Vendobionta, but debate continues on what the group as a whole represents. It is argued here that the Ediacarans constitute a broad, megascopic, paraphyletic grade of organization which overlaps the stem groups (and perhaps some crown groups) of the Porifera, Ctenophora, Cnidaria and Bilateria.

The modular organization of many Ediacarans suggests that they were fundamentally colonial organisms. The early disc‐shaped forms may have been solitary individuals, perhaps with a choanoflagellate or simple sponge‐like grade of organization; the modular forms may represent bud colonies of those entities. The more complex fronds, as well as other segmented and bilaterally symmetrical Ediacarans, seem to exhibit a trend toward higher levels of integration and individuation. This trend is comparable to those observed among more recent colonial organisms. Interpretation of modular Ediacarans as colonial organisms leads to a new perspective on the evolution of metazoans. It suggests that the earliest solitary Ediacarans furnished a framework for the development of cell and tissue specialization, including the formation of epithelia and complex connective tissues. Later colonial forms provided a mechanism to increase nested or hierarchical complexity, through duplication, integration, and individuation. Early acquisition of complexity had a profound impact on the subsequent evolution of metazoan body plans.

The Ediacarans seem to have evolved the range of colonial forms required to give rise to the radiation of complex bilaterians in the Cambrian. If this is true, it obviates the need to postulate the existence of the microscopic, acoelomate ancestors of basal metazoan taxa that are required by prevailing hypotheses bearing on the early evolution of the Metazoa.     

A Brief Review of Metazoan Phylogeny and Future Prospects in Hox-Research

Underlying any analysis on the evolution of development is aphylogenetic framework, whether explicitly stated or implied.As such, differing views on phylogenetic relationships leadto variable interpretations of how developmental mechanismshave changed through time. Over the past decade, many long-standinghypotheses about animal evolution have been questioned causingsubstantial changes in the assumed phylogenetic framework underlyingcomparative developmental studies. Current hypotheses aboutearly metazoan history suggest that three, not two, major lineagesof bilateral animals originated in the Precambrian: the Deuterostomes(e.g., seastars, acorn worms, and vertebrates), the Ecdysozoans(e.g., nematodes and arthropods), and the Lophotrochozoans (e.g.,annelids, mollusks, and lophophorates). Although informationin Hox-genes bears directly on our understanding of early metazoanevolution and the formation of body plans, research effort hasbeen focused primarily on two taxa, insects and vertebrates.By sampling a greater diversity of metazoan taxa and takingadvantage of biotechnological advances in genomics, we willnot only learn more about metazoan phylogeny, but will alsogain valuable insight as to the key evolutionary forces thatestablished and maintained metazoan bauplans.     

THE IMPORTANCE OF PREADAPTED GENOMES IN THE ORIGIN OF THE ANIMAL BODYPLANS AND THE CAMBRIAN EXPLOSION

The genomes of taxa whose stem lineages branched early in metazoan history, and of allied protistan groups, provide a tantalizing outline of the morphological and genomic changes that accompanied the origin and early diversifications of animals. Genome comparisons show that the early clades increasingly contain genes that mediate development of complex features only seen in later metazoan branches. Peak additions of protein‐coding regulatory genes occurred deep in the metazoan tree, evidently within stem groups of metazoans and eumetazoans. However, the bodyplans of these early‐branching clades are relatively simple. The existence of major elements of the bilaterian developmental toolkit in these simpler organisms implies that these components evolved for functions other than the production of complex morphology, preadapting the genome for the morphological differentiation that occurred higher in metazoan phylogeny. Stem lineages of the bilaterian phyla apparently required few additional genes beyond their diploblastic ancestors. As disparate bodyplans appeared and diversified during the Cambrian explosion, increasing complexity was accommodated largely through changes in cis‐regulatory networks, accompanied by some additional gene novelties. Subsequently, protein‐coding genic richness appears to have essentially plateaued. Some genomic evidence suggests that similar stages of genomic evolution may have accompanied the rise of land plants.     

Targeted genomic detection of biosynthetic pathways: anaerobic production of hopanoid biomarkers by a common sedimentary microbe

The lipid biomarker principle requires that preservable molecules (molecular fossils) carry specific taxonomic, metabolic, or environmental information. Historically, an empirical approach was used to link specific taxa with the compounds they produce. The lipids extracted from numerous, but randomly cultured species provided the basis for the interpretation of biomarkers in both modern environments and in the geological record. Now, with the rapid sequencing of hundreds of microbial genomes, a more focused genomic approach can be taken to test phylogenetic patterns and hypotheses about the origins of biomarkers. Candidate organisms can be selected for study on the basis of genes that encode proteins fundamental to the synthesis of biomarker compounds. Hopanoids, a class of pentacyclic triterpenoid lipid biomarkers, provide an illustrative example. For many years, interpretations of biomarker data were made with the assumption that hopanoids are produced only by aerobic organisms. However, the recent discovery of ¹³C‐depleted hopanoids in environments undergoing anaerobic methane oxidation and in enrichment cultures of anammox planctomycetes indicates that some hopanoids are produced anaerobically. To further examine the potential distribution of hopanoid biosynthesis by anaerobes, we searched publicly available genomic databases for the presence of squalene‐hopene cyclase genes in known obligate or facultative anaerobes. Here we present evidence that Geobacter sulfurreducens, Geobacter metallireducens, and Magnetospirillum magnetotacticum, all bacteria common in anoxic environments, have the appropriate genes for hopanoid biosynthesis. We further show that these data accurately predict that G. sulfurreducens does produce a variety of complex hopanoids under strictly anaerobic conditions in pure culture.     

The rise of bilaterians: a few closing comments

Freeman (2009, 2010) argue that Ediacara “faunas” should be analysed using “promorphologies” of extant animals, that rangeomorphs and erniettomorphs are colonial animals, and that Vernanimalcula is a bilaterian animal. Recent studies of Ediacara fossils have provided multiple lines of evidence that these fossils represent a sample of phylogenetically diverse marine organisms that included crown-group animals as well as stem-group animals and non-animals. Thus, it is inappropriate to analyse Ediacara fossils using “promorphologies” of extant animals. The interpretation of rangeomorphs and erniettomorphs as colonial animals is inconsistent with the functional morphologies of these Ediacara fossils. Although Vernanimalcula is a fossil, the purported germ layers of Vernanimalcula are of diagenetic origin and there is no morphological evidence in support of its bilaterian affinity.     

Diverse small spinose acritarchs from the Ediacaran Doushantuo Formation, South China

The Ediacaran Doushantuo Formation in South China is underlain by the Cryogenian Nantuo Formation (glacial rocks) and overlain by the late Ediacaran Dengying Formation. It is characterized by well-preserved, large (normally >100 μm in size) spinose acritarchs (LSAs), which have been shown to be probably the only useful biostratigraphic tool for the global correlation of the early- and middle-Ediacaran. Acritarchs are organic microfossils normally known as single-celled eukaryotic organisms (protists). Although recent research suggests that some large spinose acritarchs may represent diapause egg cysts of metazoans, the biological affinities of the Ediacaran spinose acritarchs, especially for those displaying remarkable size ranges, are still debatable.Recently, smaller specimens of the Ediacaran spinose acritarchs have been found in cherts and phosphorites of the Doushantuo Formation in South China. Many described Ediacaran spinose acritarch taxa display large size variation (from tens to hundreds of microns in vesicle diameter), but some taxa only have smaller (<70 μm) specimens. The morphological comparison with Paleozoic counterparts indicates that some Ediacaran spinose acritarchs may have phylogenetic affinity to eukaryotic algae. More evidence, including wall ultra-structure, geochemical analysis and comparison with modern analogs, is needed to understand the biological affinity of the Ediacaran spinose acritarchs. The remarkable radiation of planktonic protists, characterized by abundant, diverse spinose acritarchs, occurred as early as in the late Neoproterozoic, i.e., 40–60 million years earlier than previously thought.     

Bony labyrinth morphology in early neopterygian fishes (Actinopterygii: Neopterygii)

Endocasts of the osseous labyrinth have the potential to yield information about both phylogenetic relationships and ecology. Although bony labyrinth morphology is well documented in many groups of fossil vertebrates, little is known for early Neopterygii, the major fish radiation containing living teleosts, gars and the bowfin. Here, we reconstruct endocasts of the bony labyrinth and associated structures for a sample of Mesozoic neopterygian fishes using high‐resolution computed tomography. Our sample includes taxa unambiguously assigned to either the teleost (Dorsetichthys, “Pholidophorus,” Elopoides) and holostean (“Aspidorynchus,” “Caturus,” Heterolepidotus) total‐groups, as well as examples of less certain phylogenetic position (an unnamed parasemionotid and Dapedium). Our models provide a test of anatomical interpretations for forms where bony labyrinths were reconstructed based on destructive tomography (“Caturus”) or inspection of the lateral wall of the cranial chamber (Dorsetichthys), and deliver the first detailed insights on inner ear morphology in the remaining taxa. With respect to relationships, traits apparent in the bony labyrinth and associated structures broadly support past phylogenetic hypotheses concerning taxa agreed to have reasonably secure systematic placements. Inner ear morphology supports placement of Dapedium with holosteans rather than teleosts, while preserved structure in the unnamed parasemionotid is generalized to the degree that it provides no evidence of close affinity with either of the crown neopterygian lineages. This study provides proof‐of‐concept for the systematic utility of the inner ear in neopterygians that, in combination with similar findings for earlier‐diverging actinopterygian lineages, points to the substantial potential of this anatomical system for addressing the longstanding questions in the relationships of fossil ray‐finned fishes to one another and living groups. J. Morphol. 279:426–440, 2018. © 2016 Wiley Periodicals, Inc.     

The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution

The earliest evolution of the animals remains a taxing biological problem, as all extant clades are highly derived and the fossil record is not usually considered to be helpful. The rise of the bilaterian animals recorded in the fossil record, commonly known as the ‘Cambrian explosion’, is one of the most significant moments in evolutionary history, and was an event that transformed first marine and then terrestrial environments. We review the phylogeny of early animals and other opisthokonts, and the affinities of the earliest large complex fossils, the so‐called ‘Ediacaran’ taxa. We conclude, based on a variety of lines of evidence, that their affinities most likely lie in various stem groups to large metazoan groupings; a new grouping, the Apoikozoa, is erected to encompass Metazoa and Choanoflagellata. The earliest reasonable fossil evidence for total‐group bilaterians comes from undisputed complex trace fossils that are younger than about 560 Ma, and these diversify greatly as the Ediacaran–Cambrian boundary is crossed a few million years later. It is generally considered that as the bilaterians diversified after this time, their burrowing behaviour destroyed the cyanobacterial mat‐dominated substrates that the enigmatic Ediacaran taxa were associated with, the so‐called ‘Cambrian substrate revolution’, leading to the loss of almost all Ediacara‐aspect diversity in the Cambrian. Why, though, did the energetically expensive and functionally complex burrowing mode of life so typical of later bilaterians arise? Here we propose a much more positive relationship between late‐Ediacaran ecologies and the rise of the bilaterians, with the largely static Ediacaran taxa acting as points of concentration of organic matter both above and below the sediment surface. The breaking of the uniformity of organic carbon availability would have signalled a decisive shift away from the essentially static and monotonous earlier Ediacaran world into the dynamic and burrowing world of the Cambrian. The Ediacaran biota thus played an enabling role in bilaterian evolution similar to that proposed for the Savannah environment for human evolution and bipedality. Rather than being obliterated by the rise of the bilaterians, the subtle remnants of Ediacara‐style taxa within the Cambrian suggest that they remained significant components of Phanerozoic communities, even though at some point their enabling role for bilaterian evolution was presumably taken over by bilaterians or other metazoans. Bilaterian evolution was thus an essentially benthic event that only later impacted the planktonic environment and the style of organic export to the sea floor.