Infaunal augurs of the Cambrian explosion: An Ediacaran trace fossil assemblage from Nevada,USA

Morphologically complex trace fossils, recording the infaunal activities of bilaterian animals, are common in Phanerozoic successions but rare in the Ediacaran fossil record. Here, we describe a trace fossil assemblage from the lower Dunfee Member of the Deep Spring Formation at Mount Dunfee (Nevada, USA), over 500 m below the Ediacaran–Cambrian boundary. Although millimetric in scale and largely not fabric‐disruptive, the Dunfee assemblage includes complex and sediment‐penetrative trace fossil morphologies that are characteristic of Cambrian deposits. The Dunfee assemblage records one of the oldest documented instances of sediment‐penetrative infaunalization, corroborating previous molecular, ichnologic, and paleoecological data suggesting that crown‐group bilaterians and bilaterian‐style ecologies were present in late Ediacaran shallow marine ecosystems. Moreover, Dunfee trace fossils co‐occur with classic upper Ediacaran tubular body fossils in multiple horizons, indicating that Ediacaran infauna and epifauna coexisted and likely formed stable ecosystems.     

The earliest fossil record of the animals and its significance

The fossil record of the earliest animals has been enlivened in recent years by a series of spectacular discoveries, including embryos, from the Ediacaran to the Cambrian, but many issues, not least of dating and interpretation, remain controversial. In particular, aspects of taphonomy of the earliest fossils require careful consideration before pronouncements about their affinities. Nevertheless, a reasonable case can now be made for the extension of the fossil record of at least basal animals (sponges and perhaps cnidarians) to a period of time significantly before the beginning of the Cambrian. The Cambrian explosion itself still seems to represent the arrival of the bilaterians, and many new fossils in recent years have added significant data on the origin of the three major bilaterian clades. Why animals appear so late in the fossil record is still unclear, but the recent trend to embrace rising oxygen levels as being the proximate cause remains unproven and may even involve a degree of circularity.     

Vestiges of a beginning? Paleontological and geochemical constraints on early animal evolution

Inspired by molecular clock estimates, some biologists have proposed that animals in general, and bilaterian metazoans in particular, began to diverge substantially earlier than fossils indicate. Balavoine and Adoutte [Science 280 (1998) 397] specifically hypothesized that the Cambrian explosion documents parallel radiations within three major bilaterian clades that diverged from one another relatively early in the Neoproterozoic Era. The geological record is permissive with respect to such hypotheses, but not encouraging. The earliest evolution of animals certainly took place before the initial appearance of phosphatic animal microfossils or Ediacaran macrofossils, but bilaterian clades need not have been part of this metazoan “pre-history”. Alternatively, the evolution of large size, made possible by late Neoproterozoic oxygen increase, may have provided the selective environment in which stem bilaterians differentiated. Cambrian events per se appear to have begun in the wake of environmental perturbation and accompanying extinction near the Proterozoic–Cambrian boundary.     

The ‘biomineralization toolkit’ and the origin of animal skeletons

Biomineralized skeletons are widespread in animals, and their origins can be traced to the latest Ediacaran or early Cambrian fossil record, in virtually all animal groups. The origin of animal skeletons is inextricably linked with the diversification of animal body plans and the dramatic changes in ecology and geosphere–biosphere interactions across the Ediacaran–Cambrian transition. This apparent independent acquisition of skeletons across diverse animal clades has been proposed to have been driven by co‐option of a conserved ancestral genetic toolkit in different lineages at the same time. This ‘biomineralization toolkit’ hypothesis makes predictions of the early evolution of the skeleton, predictions tested herein through a critical review of the evidence from both the fossil record and development of skeletons in extant organisms. Furthermore, the distribution of skeletons is here plotted against a time‐calibrated animal phylogeny, and the nature of the deep ancestors of biomineralizing animals interpolated using ancestral state reconstruction. All these lines of evidence point towards multiple instances of the evolution of biomineralization through the co‐option of an inherited organic skeleton and genetic toolkit followed by the stepwise acquisition of more complex skeletal tissues under tighter biological control. This not only supports the ‘biomineralization toolkit’ hypothesis but also provides a model for describing the evolution of complex biological systems across the Ediacaran–Cambrian transition.     

Bioturbation in matgrounds at Lake Bogoria in the Kenya Rift Valley: implications for interpreting the heterogeneous early Cambrian seafloor

Modern burrowing organisms feed on microbial organic matter in matgrounds near hot springs on the margins of Lake Bogoria, a saline alkaline lake in the Kenya Rift Valley. The burrowers produce a low-diversity trace assemblage similar to those produced by undermat miners during the Ediacaran–Cambrian transition. Despite obvious differences in body plans and phylogenetic affinities, these modern animals feed on microbes in similar ways to those inferred for primitive bilaterians. With increasing distance from hot-spring vents, outflow channels and adjacent matgrounds, the diversity and depth of the traces increase and mixgrounds become dominant. This modern extreme environment gives clues for interpreting the heterogeneous early Cambrian seafloor, with: (1) the restriction of ‘pre-agronomic revolution’ matground substrates; and (2) expansion of adjacent ‘post-agronomic revolution’ mixground areas.     

Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians

The Ediacaran Doushantuo biota has yielded fossils that include the oldest widely accepted record of the animal evolutionary lineage, as well as specimens with alleged bilaterian affinity. However, these systematic interpretations are contingent on the presence of key biological structures that have been reinterpreted by some workers as artefacts of diagenetic mineralization. On the basis of chemistry and crystallographic fabric, we characterize and discriminate phases of mineralization that reflect: (i) replication of original biological structure, and (ii) void-filling diagenetic mineralization. The results indicate that all fossils from the Doushantuo assemblage preserve a complex mélange of mineral phases, even where subcellular anatomy appears to be preserved. The findings allow these phases to be distinguished in more controversial fossils, facilitating a critical re-evaluation of the Doushantuo fossil assemblage and its implications as an archive of Ediacaran animal diversity. We find that putative subcellular structures exhibit fabrics consistent with preservation of original morphology. Cells in later developmental stages are not in original configuration and are therefore uninformative concerning gastrulation. Key structures used to identify Doushantuo bilaterians can be dismissed as late diagenetic artefacts. Therefore, when diagenetic mineralization is considered, there is no convincing evidence for bilaterians in the Doushantuo assemblage.     

寒武纪早期岩家河生物群:研究进展和展望*

埃迪卡拉纪-寒武纪转换时期动物的起源、演化和"寒武纪大爆发"一直是国际古生物学界研究的热点问题,其中寒武纪早期小壳化石群与埃迪卡拉纪化石群和寒武纪早期澄江化石库之间的内在关系是古生物学界研究的难题,其主要原因是寒武纪早期与小壳化石群伴生的宏体动、植物化石的缺乏。发现于峡东地区的寒武纪早期岩家河生物群填补了这一缺失环节,该生物群包含宏体动物、宏观藻类、小壳化石、球形化石(可能的胚胎化石)、微古植物和蓝菌类等化石,部分宏体化石显示了从埃迪卡拉纪向寒武纪过渡色彩。化石保存方式有碳质膜、黄铁矿化、磷酸盐化、硅化。因此对岩家河生物群生物多样性和埋藏学进行综合研究,将可提供纽芬兰世(梅树村期)碳酸盐台地—碳酸盐台地内部的局部凹陷盆地相的一个较完整的生物景观图,对探索"寒武纪大爆发主幕"前夕生物的辐射、演化模式及保存机制具有重要的科学意义。     

湖北三峡地区埃迪卡拉系灯影组“蝌蚪状”遗迹化石*

遗迹化石是埃迪卡拉纪存在两侧对称动物最有力的证据。但多数埃迪卡拉纪遗迹化石为简单、水平的表面爬迹或潜穴。在湖北三峡地区灯影组石板滩段含典型埃迪卡拉软躯体化石的地层中新发现一类形态特别的化石,呈蝌蚪状,一端膨大,一端细管状。通过对化石形态、同位素分析以及沉积学特征的研究,说明该化石为遗迹化石,而不是实体化石。蝌蚪状化石为一种复合迹,垂向活动形成球状的膨大端,平行藻席层活动形成近于水平的潜穴,反映了造迹生物垂向切穿藻席层并沿藻席层进行觅食的行为。该发现说明了在埃迪卡拉纪晚期已有两侧对称动物开始形成较为复杂的潜穴。     

SKELETAL MICROSTRUCTURE INDICATES CHANCELLORIIDS AND HALKIERIIDS ARE CLOSELY RELATED

Abstract: Chancelloriids are problematic, sac‐like animals whose sclerites are common in Cambrian fossil assemblages. They look like sponges, but were united with the slug‐like halkieriids in the group Coeloscleritophora Bengtson and Missarzhevsky, 1981 based on a unique mode of sclerite construction. Because their body plans are so different, this proposal has never been well accepted, but detailed study of their sclerite microstructure presented here provides additional support for this grouping. Both taxa possess walls composed of a thin, probably organic, sheet overlying a single layer of aragonite fibres orientated parallel to the long axis of the sclerite. In all halkieriids and in the chancelloriid genus Archiasterella Sdzuy, 1969 , bundles of these fibres form inclined projections on the upper surface of the sclerite giving it a scaly appearance. On the lower surface of the sclerite, the projections are absent. This microstructure appears to be unique to chancelloriids, halkieriids, and their relatives, siphogonuchitids and sachitids. (The sclerites of another putative halkieriid relative, Wiwaxia Walcott, 1911 , are unmineralized, making direct comparisons impossible.) Thus, similarity both at the level of sclerite construction and the level of sclerite microstructure suggests that chancelloriid, halkieriid, sachitid, and siphogonuchitid sclerites are homologous. The difference in chancelloriid and halkieriid body plans can be resolved in two ways. Chancelloriids either represent a derived condition exhibiting complete loss of bilaterian characters or they represent the ancestral condition from which the bilaterally symmetric halkieriids, and the Bilateria as a whole, derived. The latter interpretation, proposed by Bengtson (2005) , implies that coeloscleritophoran sclerites (‘coelosclerites’) are a plesiomorphy of the Bilateria, lost or transformed in descendent lineages. Given that mineralized coelosclerites appear in the fossil record no earlier than c. 542 Ma, this in turn implies either that the Ediacaran record of bilaterians has been misinterpreted or that coelosclerite preservability increased at the beginning of the Cambrian Period. The former is difficult to reconcile with Ediacaran trace and body fossil evidence, but the latter may be possible, reflecting either independent mineralization of organic‐walled sclerites in chancelloriids and halkieriids or the opening of a taphonomic window that favours coelosclerite preservation.     

The Precambrian emergence of animal life: a geobiological perspective

The earliest record of animals (Metazoa) consists of trace and body fossils restricted to the last 35 Myr of the Precambrian. It has been proposed that animals arose much earlier and underwent significant evolution as a cryptic fauna; however, the need for any unrecorded prelude of significant duration has been disputed. In this context, we consider recent published research on the nature and chronology of the earliest fossil record of metazoans and on the molecular‐based analysis that yielded older dates for the appearance of major animal groups. We review recent work on the climatic, geochemical, and ecological events that preceded animal fossils and consider their portent for metazoan evolution. We also discuss inferences about the physiology and gene content of the last common ancestor of animals and their closest unicellular relatives. We propose that the recorded Precambrian evolution of animals includes three intervals of advancement that begin with sponge‐grade organisms, and that any preceding cryptic fauna would be no more complex than sponges. The molecular data do not require that more complex animals appeared well before the recognized fossil record; nor, however, do they rule the possibility out, particularly if the interval of simpler metazoan ancestors lasted no more than about 100 or 200 Myr. The geological record of abrupt changes in climate, biogeochemistry, and phytoplankton diversity can be taken to be the result of changes in the carbon cycle triggered by the appearance and diversification of metazoans in an organic carbon‐rich ocean, but as yet no compelling evidence exists for this interpretation. By the end of this cryptic period, animals would already have possessed sophisticated systems of cell–cell signalling, adhesion, apoptosis, and segregated germ cells, possibly with a rudimentary body plan based on anterior–posterior organization. The controls on the timing and tempo of the earliest steps in metazoan evolution are unknown, but it seems likely that oxygen was a key factor in later diversification and increase in body size. We consider several recent scenarios describing how oxygen increased near the end of the Precambrian and propose that grazing and filter‐feeding animals depleted a marine reservoir of suspended organic matter, releasing a microbial ‘clamp’ on atmospheric oxygen.     

The dawn of bilaterian animals: the case of acoelomorph flatworms

The origin of the bilaterian metazoans from radial ancestors is one of the biggest puzzles in animal evolution. A way to solve it is to identify the nature and main features of the last common ancestor of the bilaterians (LCB). Recent progress in molecular phylogeny has shown that many platyhelminth flatworms, regarded for a long time as basal bilaterians, now belong to the lophotrochozoan protostomates. In contrast, the LCB is now considered a complex organism bearing several features of modern bilaterians. Here we discuss an alternative view, in which acoelomorph (Acoela + Nemertodermatida) flatworms, which do not belong to the Platyhelminthes, represent the earliest extant bilaterian clade. Sequences from ribosomal and other nuclear genes, Hox cluster genes, and reinterpretation of some morphological features strongly support the basal position of acoelomorphs arguing against a complex LCB. This reconstruction backs the old planuloid-acoeloid hypothesis and may help our understanding of the evolution of body axes, Hox genes and the Cambrian explosion.     

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.     

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.     

Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form

We examine terminal addition, the process of addition of serial elements in a posterior subterminal growth zone during animal development, across modern taxa and fossil material. We argue that terminal addition was the basal condition in Bilateria, and that modification of terminal addition was an important component of the rapid Cambrian evolution of novel bilaterian morphology. We categorize the often-convergent modifications of terminal addition from the presumed ancestral condition. Our focus on terminal addition and its modification highlights trends in the history of animal evolution evident in the fossil record. These trends appear to be the product of departure from the initial terminal addition state, as is evident in evolutionary patterns within-fossil groups such as trilobites, but is also more generally related to shifts in types of morphologic change through the early Phanerozoic. Our argument is contingent on dates of metazoan divergence that are roughly convergent with the first appearance of metazoan fossils in the latest Proterozoic and Cambrian, as well as on an inference of homology of terminal addition across bilaterian Metazoa.     

Resolving Terreneuvian stratigraphy in subtidal–intertidal carbonates: palaeontological and chemostratigraphical evidence from the Turukhansk Uplift,Siberian Platform

Both diverse assemblages of small skeletal fossils and a representative chemostratigraphical record make the Siberian Platform widely regarded as one of the key regions for the reconstruction of global biotic and abiotic events in the late Ediacaran and early Cambrian. However, the wide distribution of intertidal–subtidal facies in the Ediacaran–Cambrian transitional strata of the central and southwestern Siberian Platform (Turukhansk–Irkutsk–Olekma facies region) produces a dramatic depletion of the palaeontological record and considerably limits their age‐calibration and long‐distance correlation. We report new lithological, palaeontological and carbonate carbon‐isotope data for the Ediacaran–Cambrian sections of the Turukhansk Uplift (northwestern Siberian Platform, western facies region). These data provide a robust framework for the chemostratigraphical correlation of the western facies region with sections of the transitional and eastern regions of the Siberian Platform and further confirms a depositional hiatus at the base of the Tommotian Stage in the stratotype section (Aldan River, SE Siberia). The carbon‐isotope curve from the Turukhansk Uplift sections correlates positively with the most chemostratigraphically representative Ediacaran–Cambrian sections (Siberia, Morocco, South China). It records major carbon‐isotope oscillations globally recognized in the lower Cambrian, enabling localization of the Fortunian and Cambrian Stage 2 boundaries in the Platonovskaya Formation. Although there is extreme paucity and poor preservation of the small skeletal fossils in the western facies region, we report individual Barskovia, Blastulospongia and chancelloriid sclerites from the Platonovskaya Formation. A combination of palaeontological and chemostratigraphical data suggests the base of P. antiqua Assemblage Zone is located in the middle Platonovskaya Formation. The earliest spiral gastropods probably occurred at ~541 Ma, as demonstrated by the discovery of a specimen of Barskovia near the base of the large negative excursion in the lower Platonovskaya Formation, correlated with the BACE negative carbon‐isotope peak in the sections of the Yangtze Platform.     

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.     

Trace fossils from arenig flysch sediments of eire and their bearing on the early colonisation of the deep seas

A sequence of Lower Ordovician (Arenig) turbidites in Co. Wexford, Eire, has yielded one of the earliest diverse ichnofaunas yet recorded from deep water sediments comprising: Chondrites, Glockerichnus, Gordia, Helminthopsis, Lorenzinia, Neonereites, Palaeophycus, Paleodictyon, Planolites, Sublorenzinia, Taenidium, Taphrhelminthopsis, Teichichnus and Tomaculum. This ichnofauna is critical in any analysis of the colonisation of the deep seas by trace fossil‐producing animals.

A world‐wide review shows that the earliest trace fossils are mainly from Late Precambrian shelf sea environments, but many more evolved during very rapid diversification in the pre‐trilobite Lower Cambrian.

There was little increase in diversity in shallow water after the Lower Cambrian but a progressive colonisation of the deep ocean took place and this accelerated during the Ordovician, when the main lineages of deep sea trace fossils were established there. Rosetted, patterned, meandering and simple spiral forms evolved in shallow water in the Upper Precambrian and pre‐trilobite Lower Cambrian and only later migrated into the deep sea, whereas complex, closely programmed, spiral traces may have evolved there.     

Reappraising the early evidence of durophagy and drilling predation in the fossil record: implications for escalation and the Cambrian Explosion

The Cambrian Explosion is arguably the most extreme example of a biological radiation preserved in the fossil record, and studies of Cambrian Lagerstätten have facilitated the exploration of many facets of this key evolutionary event. As predation was a major ecological driver behind the Explosion – particularly the radiation of biomineralising metazoans – the evidence for shell crushing (durophagy), drilling and puncturing predation in the Cambrian (and possibly the Ediacaran) is considered. Examples of durophagous predation on biomineralised taxa other than trilobites are apparently rare, reflecting predator preference, taphonomic and sampling biases, or simply lack of documentation. The oldest known example of durophagy is shell damage on the problematic taxon Mobergella holsti from the early Cambrian (possibly Terreneuvian) of Sweden. Using functional morphology to identify (or perhaps misidentify) durophagous predators is discussed, with emphasis on the toolkit used by Cambrian arthropods, specifically the radiodontan oral cone and the frontal and gnathobasic appendages of various taxa. Records of drill holes and possible puncture holes in Cambrian shells are mostly on brachiopods, but the lack of prey diversity may represent either a true biological signal or a result of various biases. The oldest drilled Cambrian shells occur in a variety of Terreneuvian‐aged taxa, but specimens of the ubiquitous Ediacaran shelly fossil Cloudina also show putative drilling traces. Knowledge on Cambrian shell drillers is sorely lacking and there is little evidence or consensus concerning the taxonomic groups that made the holes, which often leads to the suggestion of an unknown ‘soft bodied driller’. Useful methodologies for deciphering the identities and capabilities of shell drillers are outlined. Evidence for puncture holes in Cambrian shelly taxa is rare. Such holes are more jagged than drill holes and possibly made by a Cambrian ‘puncher’. The Cambrian arthropod Yohoia may have used its frontal appendages in a jack‐knifing manner, similar to Recent stomatopod crustaceans, to strike and puncture shells rapidly. Finally, Cambrian durophagous and shell‐drilling predation is considered in the context of escalation – an evolutionary process that, amongst other scenarios, involves predators (and other ‘enemies’) as the predominant agents of natural selection. The rapid increase in diversity and abundance of biomineralised shells during the early Cambrian is often attributed to escalation: enemies placed selective pressure on prey, forcing phenotypic responses in prey and, by extension, in predator groups over time. Unfortunately, few case studies illustrate long‐term patterns in shelly fossil morphologies that may reflect the influence of predation throughout the Cambrian. More studies on phenotypic change in hard‐shelled lineages are needed to convincingly illustrate escalation and the responses of prey during the Cambrian.