Nicholas J. Butterfield

Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes

Abstract Multicellular filaments from the ca. 1200-Ma Hunting Formation (Somerset Island, arctic Canada) are identified as bangiacean red algae on the basis of diagnostic cell-division patterns. As the oldest taxonomically resolved eukaryote on record Bangiomorpha pubescens n. gen. n. sp. provides a key datum point for constraining protistan phylogeny. Combined with an increasingly resolved record of other Proterozoic eukaryotes, these fossils mark the onset of a major protistan radiation near the Mesoproterozoic/Neoproterozoic boundary. Differential spore/gamete formation shows Bangiomorpha pubescens to have been sexually reproducing, the oldest reported occurrence in the fossil record. Sex was critical for the subsequent success of eukaryotes, not so much for the advantages of genetic recombination, but because it allowed for complex multicellularity. The selective advantages of complex multicellularity are considered sufficient for it to have arisen immediately following the appearance of sexual reproduction. As such, the most reliable proxy for the first appearance of sex will be the first stratigraphic occurrence of complex multicellularity. Bangiomorpha pubescens is the first occurrence of complex multicellularity in the fossil record. A differentiated basal holdfast structure allowed for positive substrate attachment and thus the selective advantages of vertical orientation; i.e., an early example of ecological tiering. More generally, eukaryotic multicellularity is the innovation that established organismal morphology as a significant factor in the evolutionary process. As complex eukaryotes modified, and created entirely novel, environments, their inherent capacity for reciprocal morphological adaptation, gave rise to the “biological environment” of directional evolution and “progress.” The evolution of sex, as a proximal cause of complex multicellularity, may thus account for the Mesoproterozoic/Neoproterozoic radiation of eukaryotes.

Exceptional Fossil Preservation and the Cambrian Explosion

Abstract Exceptionally preserved, non-biomineralizing fossils contribute importantly to resolving details of the Cambrian explosion, but little to its overall patterns. Six distinct “types” of exceptional preservation are identified for the terminal Proterozoic-Cambrian interval, each of which is dependent on particular taphonomic circumstances, typically restricted both in space and time. Taphonomic pathways yielding exceptional preservation were particularly variable through the Proterozoic-Cambrian transition, at least in part a consequence of contemporaneous evolutionary innovations. Combined with the reasonably continuous record of “Doushantuo-type preservation,” and the fundamentally more robust records of shelly fossils, phytoplankton cysts and trace fossils, these taphonomic perturbations contribute to the documentation of major evolutionary and biogeochemical shifts through the terminal Proterozoic and early Cambrian. Appreciation of the relationship between taphonomic pathway and fossil expression serves as a useful tool for interpreting exceptionally preserved, often problematic, early Cambrian fossils. In shale facies, for example, flattened non-biomineralizing structures typically represent the remains of degradation-resistant acellular and extracellular “tissues” such as chaetae and cuticles, whereas three-dimensional preservation represents labile cellular tissues with a propensity for attracting and precipitating early diagenetic minerals. Such distinction helps to identify the acuticular integument of hyolithids, the chaetae-like nature of Wiwaxia sclerites, the chaetognath-like integument of Amiskwia, the midgut glands of various Burgess Shale arthropods, and the misidentification of deposit-feeding arthropods in the Chengjiang biota. By the same reasoning, putative lobopods in the Sirius Passet biota and putative deuterostomes in the Chengiang biota are better interpreted as arthropods.

Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen

A fossil Lagerstatte from the 700–750 Ma old Svanbergfjellet Formation of northeastern Spitsbergen offers a substantially enhanced view of late Proterozoic paleobiology. Fossils occur primarily as Organic-walled compressions in shales and permineralizations in chert: secondary modes of preservation include bedding-plane imprints and mineral replacements in apatite and goethite (?). The depositional setting of all fossiliferous horizons is broadly peritidal with highest taxonomic diversity occurring in shallow subtidal settings; the details of included fossil assemblages contribute to improved paleoecological resolution. The often distinct constituents of shale-and chert-hosted fossil assemblages appear to be a product of both paleoenvironment and fundamentally dissimilar taphonomic pathways, such that only forms with inferred wide ecological tolerance appear in both. Consideration of taphonomic processes also provides a variety of useful taxonomic insights, on the one hand permitting some resolution of so-called wastebasket taxa. such as Chuaria, and on the other acknowledging the taxonomic disparity that can occur in simple forms like Siphonophycus and Oscillatoriopsis. True multicellular (including coenocytic) eukaryotes are a conspicuous Component of the Svanbergfjellet assemblage: of eight distinct taxa, one can be identified as a coenobial/colonial chlorococcalean and three as filamentous siphonocladaleans (Chlorophyta). Other forms are problematic, but several show significant cell, or possibly tissue, differentiation. A review of Proterozoic multicellular organisms reveals that a coenocytic grade of organization was common among early metaphytes and supports the view (that a cellularity is a derived condition in many ‘multicellular’ lineages. Nineteen acritarch taxa are preserved in the Svanbergfjellet sediments. Ten of these show a readily identifiable ornamentation and contribute significantly to Neoproterozoic biostratigraphy; a world-wide and exclusively Late Riphean distribution of the acanthomorph Trachyhystrichosphaera aimika identifies it as a particularly valuable index fossil. The Svanbergfjellel fossil assemblage preserves a total of 63 distinct forms, of which 56 are treated taxonomically. As much as possible, principles of ‘natural’ taxonomy are applied, such that taphonomic and ontogenetic variants are declined separate taxonomy status. Major taxonomic revisions are offered for the acritarchs Trachyhystrichosphaera and Chuaria as well as for the prokaryotic-grade filaments: Cephalonyx, Cyanonema, Oscillatoriopsis, Palaeolyngbya, Rugossopsis, Siphonophycus, Tortunema, and Veteronostocale. Newly erected taxa include 7 new genera: Palaeastrum. Proterocladus, Pseudotawuia, Valkyria, Cerebrosphaera, Osculosphera and Pseudodendron; 14 new species in 12 genera: Palaestrum ***dyptocranum, Proterocladus major, Proterocladus minor, Proterocladus ***hermannae. Pseudodendron birenifera, Valkyria borealis, Cerebrosphaera buickii, Osculosphaera hyaline, Pseudodendron anteridium fullerne, Germinosphaera jankauskasii, Trachyhystrichosphaera polaris, Siphonophycus thulenema and thulenema and Digitus adumbrates 7 new combinations: Leiosphaeridia wimanii, Eoentophysalis croxfordii Cephlonyx geminatus. Oscillatoriopsis amadeus. Siphonophycus typicum, Siphonophycus solidum and Tortunema Wernadskii.

Strontium isotopic variations of Neoproterozoic seawater: Implications for crustal evolution

We report high precision Sr isotopic data on carbonates from the Neoproterozoic Shaler Group, Victoria Island, Northwest Territories, Canada. Lithostratigraphic correlations with the relatively well-dated Mackenzie Mountains Supergroup constrain Shaler deposition to approximately 770-880 Ma, a range corroborated by 723 +/- 3 Ma lavas that disconformably overlie Shaler carbonates and by Late Riphean microfossils within the section. Samples with low 87Rb/86Sr ratios (<0.01) were selected for Sr isotopic analysis. Delta 18O, Mn, Ca, Mg, and Sr data were used to recognize altered samples. The altered samples are characterized by high Mn/Sr (> or = 2) and variable delta 18O; most are dolomites. The data indicate that between ca. 790-850 Ma the 87Sr/86Sr ratio of seawater varied between 0.70676 and 0.70561. The samples show smooth and systematic variation, with the lowest 87Sr/86Sr value of 0.70561 at ca. 830 Ma. The low 87Sr/86Sr ratio of carbonates from the lower parts of our section is similar to a value reported for one sample from the Adrar of Mauritania (approximately 900 Ma), West African Craton. Isotopic ratios from the upper part of the Shaler section are identical to values from the lower part of the Neoproterozoic Akademikerbreen Group, Spitsbergen. Although a paucity of absolute age determinations hinders attempts at the precise correlation of Neoproterozoic successions, it is possible to draw a broad outline of the Sr isotopic composition of seawater for this period. Indeed, the Sr isotope data themselves provide a stratigraphic tool of considerable potential. Data from this study and the literature are used to construct a curve of the 87Sr/86Sr ratio of Neoproterozoic seawater. The new data reported in this study substantially improve the isotopic record of Sr in seawater for the period 790-850 Ma. The Sr isotope composition of seawater reflects primarily the balance between continental Sr input through river input and mantle input via hydrothermal circulation of seawater through mid-ocean ridges. Coupling of Nd and Sr isotopic systems allows us to model changes in seafloor spreading rates (or hydrothermal flux) and continental erosion. The Sr hydrothermal flux and the erosion rate (relative to present-day value) are modeled for the period 500-900 Ma. The results indicate that the hydrothermal flux reached a maximum value at ca. 830 Ma. In contrast, a large peak in erosion rate is indicated at ca. 570 Ma. The peaks in hydrothermal flux and erosion rate are most likely related to developments in the Pan-African and related orogenic events, whose initial development is characterized by production of juvenile crust during supercontinental break up and rifting. The time ca. 570 Ma is characterized by continent-continent collision and production of recycled crust. Sr isotope data from Proterozoic carbonates offer a valuable resource for understanding large-scale crust dynamics.

Organic preservation of non-mineralizing organisms and the taphonomy of the Burgess Shale

Organic preservation of non-mineralizing animals constitutes an important part of the paleontological record, yet the processes involved have not been investigated in detail. Organic-walled fossils are generally explicable as a coincidence of original, relatively recalcitrant, extra-cellular materials and more or less anti-biotic depositional circumstances. One of the most pervasive natural inhibitors of biodegradation results from substrate and enzyme adsorption onto, and within, clay minerals; such interactions are likely responsible for many of the organic-walled fossils preserved in clastic sediments. Close examination of the fossil Lagerstatte of the Burgess Shale (Middle Cambrian, British Columbia) reveals that most of its so-called soft-bodied fossils are composed of primary (although kerogenized) organic carbon. Their preservation can be attributed to pervasive clay-organic interactions as the organisms were transported in a moving sediment cloud and buried with all cavities and spaces permeated with fine grained clays. The organic-walled Burgess Shale fossils were studied both in petrographic thin section and isolated from the rock matrix, following careful acid maceration. Isotopic analysis of bulk organic and carbonate carbon yielded values consistent with a normal marine paleoenvironment. Anatomical and histological consideration of the enigmatic Burgess worm Amiskwia suggest that it may in fact be a chaetognath, while the putative chordate Pikaia appears not to be related to modern cephalochordates.

Oxygen, animals and oceanic ventilation: an alternative view.

Of all the components of biogeochemical cycles, few attract more attention than the waste product of oxygenic photosynthesis. Chemically unstable and biosynthetically dangerous, diatomic oxygen is the key ingredient in aerobic metabolism, and a prerequisite for the evolution of large complex organisms that define the modern biosphere. Exactly how much they require is only loosely constrained, but Catling et al . (2005) suggest something in the order of 10 3 –10 4 pascals [Pa] ( ≈ 1–10% atmospheric partial pressure [ p O 2 ]; ≈ 5–50% present atmospheric level [PAL]). Moreover, geochemical modelling indicates that p O 2 has fluctuated substantially over the course of the Phanerozoic: up to c . 35% in the late Palaeozoic, and down to perhaps 10% in the early Mesozoic (Falkowski et al ., 2005; Berner, 2006). Such shifts have been considered instrumental in directing the course of Phanerozoic evolution and extinction (Falkowski et al ., 2005; Huey & Ward, 2005; Ward et al ., 2006; Berner et al ., 2007), including the Ediacaran–Cambrian radiations of macroscopic life (Berkner & Marshall, 1965; Anbar & Knoll, 2002; Catling et al ., 2005; Holland, 2006; Canfield et al ., 2007). This is certainly a worthy hypothesis, and one that has gained an exceptionally wide following over the past decade – but a popular paradigm still needs to be tested and weighed against competing scenarios. In this editorial, I take critical look at the oxygen-evolution connection and discuss an alternative, biological explanation for geochemical signatures through the terminal Proterozoic. In the absence of direct measurements, the oxygen content of ancient atmospheres is inferred from a combination of geochemical proxies and modelling. These values, however, are accompanied by substantial error (see Berner et al ., 2007: fig. 1; Kump, 2008: fig. 2), and differing modelling assumptions yield conspicuously different results. For example, where Bergman et al . (2004) estimate the oxygen content of Mesozoic atmospheres to be continuously at or above PAL, Berner (2006) puts late Triassic/early Jurassic levels close to 50% PAL, followed by an early Cretaceous rise to more or less modern levels. Falkowski et al . (2005) also recognize an early Jurassic minimum, but with PAL not reached until the Eocene. All models are of course limited by the runaway wildfire induced at p O 2 > 35%, and lack of fire at p O 2 < 15% (Belcher & McElwain, 2008), neither of which have obtained for the past 420 million years (with the possible exception of a ‘charcoal gap’ in the late Devonian (Scott & Glasspool, 2006)). Atmospheric oxygen concentrations are more difficult to constrain in the absence of a land plant record, though the appearance of iron-retaining palaeosols at or around the 2.45 Ga ‘great oxygenation event’ marks the onset of p O 2 > 0.2% (1% PAL), and the rise of conspicuously macroscopic fossils from c . 575 Ma sets a Phanerozoic lower limit of c . 1% p O 2 or 5% PAL (Canfield, 2005; Catling et al ., 2005; Holland, 2006; Kump, 2008). Deep-sea geochemical proxies and modelling have been used to estimate an upper limit of c . 8% p O 2 (40% PAL) for most of the Proterozoic.

Probable Proterozoic fungi

Abstract A large, morphologically heterogeneous population of acanthomorphic acritarchs from the early Neoproterozoic Wynniatt Formation, Victoria Island, northwestern Canada, is ascribed to two form-genera, Tappania and Germinosphaera, but just a single natural taxon, Tappania. Analysis of Tappania morphology shows it to have been an actively growing, benthic, multicellular organism capable of substantial differentiation. Most notably, its septate, branching, filamentous processes were capable of secondary fusion, a synapomorphy of the “higher fungi.” Combined with phylogenetic, taphonomic and functional morphologic evidence, such “hyphal fusion” identifies Tappania reliably, if not conclusively, as a fungus, probably a sister group to the “higher fungi,” but more derived than the zygomycetes. The presence of Tappania in the Mesoproterozoic Roper Group of Australia extends the record of putative fungi to 1430 Ma. Along with other Proterozoic acritarchs exhibiting fungus-like characteristics (e.g., Trachyhystrichosphaera, Shuiyousphaeridium, Dictyosphaera, Foliomorpha), there is a case to be made for an extended and relatively diverse record of Proterozoic fungi.

Leanchoilia guts and the interpretation of three-dimensional structures in Burgess Shale-type fossils

Abstract The Burgess Shale arthropod Leanchoilia superlata Walcott 1912, commonly preserves a three-dimensional axial structure generally interpreted as gut contents. Thin-section examination shows this instead to be phosphatized biserially repeated midgut glands, including exceptional preservation of subcellular features. The preferential mineralization of these structures is related to their unusually high chemical reactivity and probably to an internal source of phosphate. Sub-millimetric lineations previously interpreted as annular musculature are in fact planar, sometimes radially arranged, subdivisions of these glands. Ventral rows of isolated phosphate patches appear to represent the same tissue. In extant arthropods, extensively developed midgut glands are related to a rich but infrequent diet with a primary function in storage. Their conspicuous occurrence in unambiguous fossil predators such as Sidneyia and Laggania (Anomalocaris) suggests they served a similar role in the Cambrian; by extension, their conspicuous occurrence in Leanchoilia suggests it was a predator or scavenger. Phosphatized midguts with a structure essentially indistinguishable from that of Leanchoilia are also found in Burgess Shale Odaraia, Canadaspis, Perspicaris, Sidneyia, Anomalocaris, and Opabinia. All are characterized by a distinctive sub-millimetric arrangement of planar elements that is not found in extant arthropods or trilobites, suggesting they diverged before the last common ancestor of extant forms; i.e., they represent stem-group arthropods. Three-dimensionally preserved guts are widely preserved in the Lower Cambrian Chengjiang biota but, unlike those in the Burgess Shale, appear to be filled with sediment. Although generally interpreted as evidence of deposit feeding, the form of these structures points to early permineralization of (sediment-free) midgut glands that were subsequently altered to clay minerals. There is no evidence of deposit feeding in the Chengjiang; indeed, there is a case to be made for deposit feeding not being generally exploited generally until after the Cambrian. Fossils with three-dimensionally preserved axes from the Lower Cambrian Sirius Passet biota have been interpreted as lobopodians; however, most of the putative lobopodian features find alternative interpretations as aspects of Leanchoilia-type midgut glands. Although Kerygmachela is reliably identified as a stem-group arthropod, its phylogenetic position remains unresolved owing to the non-preservation of critical external features and to the plesiomorphic nature of its Leanchoilia-type midgut.

A reassessment of the enigmatic Burgess Shale fossil Wiwaxia corrugata (Matthew) and its relationship to the polychaete Canadia spinosa Walcott

The enigmatic fossil Wiwaxia corrugata is organically preserved in the Burgess Shale (Middle Cambrian, British Columbia) and is therefore extractable by careful acid maceration of the mineralic matrix. High magnification transmitted light microscopy and SEM of macerated Wiwaxia sclerites reveal a substantial amount of previously undescribed structural and microstructural detail. Anatomical and histological comparison with modern organisms indicates that Wiwaxia sclerites are polychaete paleae (flattened setae) and that Wiwaxia was a jawed annelid broadly related to the extant polychaete families Chrysopetalidae and/or Aprhoditidae (Palmyra). Canadia spinosa, an un- contested fossil polychaete from the same beds, shows a paleal microstructure identical to that of Wiwaxia, as well as a closely comparable gross anatomy and taphonomic grade. The unique com- bination of taxonomically significant characters shared by Wiwaxia and Canadia suggest that they are more closely related to each other than either is to any other fossil or extant polychaete. Thus they constitute a separate superfamily, Canadiacea superfam. nov., in the order Phyllodocida.

A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion

Abstract A morphologically diverse assemblage of organic-walled fossils from the middle Neoproterozoic Svanbergfjellet Formation, Spitsbergen, is identified as a monospecific assemblage representing the Gongrosira-phase of a vaucheriacean xanthophyte alga. As such, it provides a range of additional criteria with which to identify fossil vaucheriaceans and confirms the identification of Palaeovaucheria in the Mesoproterozoic Lakhanda Formation. Pronounced taxonomic inflation, through the practice of form-taxonomy, suggests that overall estimates of eukaryotic diversity in the Proterozoic need to be adjusted downward. Combined with positive evidence for low levels of speciation and extended stasis, pre-Cambrian eukaryotes are seen to evolve at a fundamentally lower rate than their Phanerozoic counterparts. This slower turnover accounts for the “delayed” appearance of animals without appeal to external triggers or constraints. The Cambrian acceleration of evolutionary rates was a direct consequence of newly introduced animals, whereas the much slower overall rates of the Proterozoic imply an absence of earlier metazoans.