Robert S. Sansom

Non-random decay of chordate characters causes bias in fossil interpretation.

Exceptional preservation of soft-bodied Cambrian chordates provides our only direct information on the origin of vertebrates. Fossil chordates from this interval offer crucial insights into how the distinctive body plan of vertebrates evolved, but reading this pre-biomineralization fossil record is fraught with difficulties, leading to controversial and contradictory interpretations. The cause of these difficulties is taphonomic: we lack data on when and how important characters change as they decompose, resulting in a lack of constraint on anatomical interpretation and a failure to distinguish phylogenetic absence of characters from loss through decay. Here we show, from experimental decay of amphioxus and ammocoetes, that loss of chordate characters during decay is non-random: the more phylogenetically informative are the most labile, whereas plesiomorphic characters are decay resistant. The taphonomic loss of synapomorphies and relatively higher preservation potential of chordate plesiomorphies will thus result in bias towards wrongly placing fossils on the chordate stem. Application of these data to Cathaymyrus (Cambrian period of China) and Metaspriggina (Cambrian period of Canada) highlights the difficulties: these fossils cannot be placed reliably in the chordate or vertebrate stem because they could represent the decayed remains of any non-biomineralized, total-group chordate. Preliminary data suggest that this decay filter also affects other groups of organisms and that ‘stem-ward slippage’ may be a widespread but currently unrecognized bias in our understanding of the early evolution of a number of phyla.

Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record

The timing and sequence of events underlying the origin and early evolution of vertebrates remains poorly understood. The palaeontological evidence should shed light on these issues, but difficulties in interpretation of the non-biomineralized fossil record make this problematic. Here we present an experimental analysis of decay of vertebrate characters based on the extant jawless vertebrates (Lampetra and Myxine). This provides a framework for the interpretation of the anatomy of soft-bodied fossil vertebrates and putative cyclostomes, and a context for reading the fossil record of non-biomineralized vertebrate characters. Decay results in transformation and non-random loss of characters. In both lamprey and hagfish, different types of cartilage decay at different rates, resulting in taphonomic bias towards loss of ‘soft’ cartilages containing vertebrate-specific Col2α1 extracellular matrix proteins; phylogenetically informative soft-tissue characters decay before more plesiomorphic characters. As such, synapomorphic decay bias, previously recognized in early chordates, is more pervasive, and needs to be taken into account when interpreting the anatomy of any non-biomineralized fossil vertebrate, such as Haikouichthys, Mayomyzon and Hardistiella.

Fossilization causes organisms to appear erroneously primitive by distorting evolutionary trees

Fossils are vital for calibrating rates of molecular and morphological change through geological time, and are the only direct source of data documenting macroevolutionary transitions. Many evolutionary studies therefore require the robust phylogenetic placement of extinct organisms. Here, we demonstrate that the inevitable bias of the fossil record to preserve just hard, skeletal morphology systemically distorts phylogeny. Removal of soft part characters from 78 modern vertebrate and invertebrate morphological datasets resulted in significant changes to phylogenetic signal; it caused individual taxa to drift from their original position, predominately downward toward the root of their respective trees. This last bias could systematically inflate evolutionary rates inferred from molecular data because first fossil occurrences will not be recognised as such. Stem-ward slippage, whereby fundamental taphonomic biases cause fossils to be interpreted as erroneously primitive, is therefore a ubiquitous problem for all biologists attempting to infer macroevolutionary rates or sequences.

Soft-part anatomy of the Early Cambrian bivalved arthropods Kunyangella and Kunmingella: significance for the phylogenetic relationships of Bradoriida

Bradoriids are small bivalved marine arthropods that are widespread in rocks of Cambrian to Early Ordovician age. They comprise seven families and about 70 genera based on shield (‘carapace’) morphology. New bradoriid specimens with preserved soft-part anatomy of Kunmingella douvillei (Kunmingellidae) are reported from the Early Cambrian Chengjiang Lagerstätte of China together with, for the first time to our knowledge, a second bradoriid species with preserved soft parts, Kunyangella cheni (Comptalutidae). Kunmingella douvillei has a 10-segmented limb-bearing body with uniramous ninth and tenth appendages and a series of homogeneous, apparently (proximal parts not preserved) unspecialized post-antennal biramous limbs with setose leaf-shaped exopods. Each endopod consists of five podomeres. A presumed penultimate instar of Ky. cheni preserves remnants of three head and two trunk appendages, and the adult is reconstructed as having four head appendages. This material allows testing of the affinity of the Bradoriida. Kunmingella is identified as a stem crustacean in character-based analyses, through both morphological comparisons and cladistic reconstructions. Global parsimony analysis recovers a monophyletic Bradoriida as the sister group to crown crustaceans.

Phylogeny, classification and character polarity of the Osteostraci (Vertebrata)

Synopsis The jawless Osteostraci are the sister taxon to jawed vertebrates and, thus, are integral to understanding the evolution of gnathostomes from a jawless ancestor. Our understanding of this episode is currently hampered by incomplete knowledge of osteostracan phylogenetics and character polarity. Previous hypotheses of osteostracan intrarelations are reviewed and synthesised into two conflicting hypotheses ‐ ’Tremataspis‐basal’ versus ’Ateleaspis‐basal’ models, both related to the ancestral morphotype of the group. Previous analyses are shown to be limited in three main regards ‐ taxonomic scope, phylogenetic methodology and character polarity. To address this problem, direct observations and reconstructions were made for every osteostracan genus. This enabled a taxonomically comprehensive analysis, utilising global parsimony and out‐group analysis. The inclusion of a morphological range of taxa from both extant and extinct osteostracan‐related clades (pteraspidomorphs, galeaspids, placoderms and gnathostomes), enables a test of osteostracan polarity and character evolution. A new phylogeny and classification for the Osteostraci is proposed, identifying three main orders ‐ Benneviaspidida, Zenaspidida and Thyestiida. The ’Ateleaspis‐basal’ model is supported along with the homology of paired pectoral fins of Osteostraci and jawed vertebrates.

The origin and early evolution of the Osteostraci (Vertebrata): A phylogeny for the Thyestiida

Synopsis The Osteostraci are currently regarded as the sister taxon to jawed vertebrates and, as such, osteostracan phylogeny, notably their hypothetical ancestral morphotype, has far reaching ramifications for early vertebrate evolution. The polarity of the group and the monophyly and interrelationships of the proposed constituent clades have not been tested. Here a new phylogeny is proposed for the Thyestiida, the most controversial and informative of the five main orders of Osteostraci. A comprehensive global parsimony approach is applied for the first time. The monophyly of the group, including genera of suspected thyestiid affinities, is firmly demonstrated, as is the monophyly of some constituent groups such as the Siberian Tannuaspidinae. The phylogeny supports the proposals of Janvier (1985a‐c) and is inconsistent with previous ‘Tremataspis‐basal’ models of Osteostracan evolution. Application of the phylogeny to the stratigraphical record demonstrates an early evolution and origin for the Osteostraci and indicates a missing fossil record for the group in the Llandovery, strongly related to facies bias.

Discriminating signal from noise in the fossil record of early vertebrates reveals cryptic evolutionary history

The fossil record of early vertebrates has been influential in elucidating the evolutionary assembly of the gnathostome bodyplan. Understanding of the timing and tempo of vertebrate innovations remains, however, mired in a literal reading of the fossil record. Early jawless vertebrates (ostracoderms) exhibit restriction to shallow-water environments. The distribution of their stratigraphic occurrences therefore reflects not only flux in diversity, but also secular variation in facies representation of the rock record. Using stratigraphic, phylogenetic and palaeoenvironmental data, we assessed the veracity of the fossil records of the jawless relatives of jawed vertebrates (Osteostraci, Galeaspida, Thelodonti, Heterostraci). Non-random models of fossil recovery potential using Palaeozoic sea-level changes were used to calculate confidence intervals of clade origins. These intervals extend the timescale for possible origins into the Upper Ordovician; these estimates ameliorate the long ghost lineages inferred for Osteostraci, Galeaspida and Heterostraci, given their known stratigraphic occurrences and stem–gnathostome phylogeny. Diversity changes through the Silurian and Devonian were found to lie within the expected limits predicted from estimates of fossil record quality indicating that it is geological, rather than biological factors, that are responsible for shifts in diversity. Environmental restriction also appears to belie ostracoderm extinction and demise rather than competition with jawed vertebrates.

Bias and Sensitivity in the Placement of Fossil Taxa Resulting from Interpretations of Missing Data

The utility of fossils in evolutionary contexts is dependent on their accurate placement in phylogenetic frameworks, yet intrinsic and widespread missing data make this problematic. The complex taphonomic processes occurring during fossilization can make it difficult to distinguish absence from non-preservation, especially in the case of exceptionally preserved soft-tissue fossils: is a particular morphological character (e.g., appendage, tentacle, or nerve) missing from a fossil because it was never there (phylogenetic absence), or just happened to not be preserved (taphonomic loss)? Missing data have not been tested in the context of interpretation of non-present anatomy nor in the context of directional shifts and biases in affinity. Here, complete taxa, both simulated and empirical, are subjected to data loss through the replacement of present entries (1s) with either missing (?s) or absent (0s) entries. Both cause taxa to drift down trees, from their original position, toward the root. Absolute thresholds at which downshift is significant are extremely low for introduced absences (two entries replaced, 6% of present characters). The opposite threshold in empirical fossil taxa is also found to be low; two absent entries replaced with presences causes fossil taxa to drift up trees. As such, only a few instances of non-preserved characters interpreted as absences will cause fossil organisms to be erroneously interpreted as more primitive than they were in life. This observed sensitivity to coding non-present morphology presents a problem for all evolutionary studies that attempt to use fossils to reconstruct rates of evolution or unlock sequences of morphological change. Stem-ward slippage, whereby fossilization processes cause organisms to appear artificially primitive, appears to be a ubiquitous and problematic phenomenon inherent to missing data, even when no decay biases exist. Absent characters therefore require explicit justification and taphonomic frameworks to support their interpretation.

Preservation and phylogeny of Cambrian ecdysozoans tested by experimental decay of Priapulus

The exceptionally preserved Cambrian fossil record provides unique insight into the early evolutionary history of animals. Understanding of the mechanisms of exceptional soft tissue preservation frames all interpretations of the fauna and its evolutionary significance. This is especially true for recent interpretations of preserved nervous tissues in fossil ecdysozoans. However, models of soft tissue preservation lack empirical support from actualistic studies. Here experimental decay of the priapulid Priapulus reveal consistent bias towards rapid loss of internal non-cuticular anatomy compared with recalcitrant cuticular anatomy. This is consistent with models of Burgess Shale-type preservation and indicates that internal tissues are unlikely to be preserved with fidelity if organically preserved. This pattern, along with extreme body margin distortion, is consistent with onychophoran decay, and is therefore resolved as general for early ecdysozoans. Application of these patterns to phylogenetic data finds scalidophoran taxa to be very sensitive to taphonomically informed character coding, but not panarthropodan taxa. Priapulid decay also have unexpected relevance for interpretation of myomeres in fossil chordates. The decay data presented serve not only as a test of models of preservation but also a framework with which to interpret ecdysozoan fossil anatomies, and the subsequent evolutionary inferences drawn from them.

Unusual anal fin in a Devonian jawless vertebrate reveals complex origins of paired appendages

Jawed vertebrates (gnathostomes) have undergone radical anatomical and developmental changes in comparison with their jawless cousins (cyclostomes). Key among these is paired appendages (fins, legs and wings), which first evolved at some point on the gnathostome stem. The anatomy of fossil stem gnathostomes is, therefore, fundamental to our understanding of the nature and timing of the origin of this complex innovation. Here, we show that Euphanerops, a fossil jawless fish from the Devonian, possessed paired anal-fin radials, but no pectoral or pelvic fins. This unique condition occurs at an early stage on the stem-gnathostome lineage. This condition, and comparison with the varied condition of paired fins in other ostracoderms, indicates that there was a large amount of developmental plasticity during this episode—rather than a gradual evolution of this complex feature. Apparently, a number of different clades were exploring morphospace or undergoing multiple losses.