Early Tetrapods Research Articles

New data on Ossinodus pueri, a stem tetrapod from the Early Carboniferous of Australia

ABSTRACT Significant new material of the Early Carboniferous stem tetrapod Ossinodus pueri has been found in the Ducabrook Formation, Queensland, Australia. An articulated partial skull (including skull roof and palate) as well as isolated jugal, surangular, postsplenial, intercentra, and haemal arch elements are described for the first time. New features of the cranial material include a preopercular bone, and an entirely enclosed quadratojugal sensory canal. This canal exits from the accessory paraquadrate foramen on the inner face of the quadratojugal, suggesting that the foramen was not an opening for nerves or blood vessels to enter the skull. It is argued that enclosed sensory canals may be present but undetected in other early tetrapods. A new reconstruction of the skull and the first full body reconstruction of O. pueri show a tetrapod that appears to be quite different from the whatcheeriids, Whatcheeria and Pederpes. Two phylogenetic analyses, one in which the taxon has an intertemporal, and one in which that bone is absent, place Ossinodus differently. In the first, Ossinodus remains in the Whatcheeriidae, while in the second (in which the intertemporal is absent) it is stemward of the Whatcheeriidae, adding credence to previous suggestions that the Whatcheeriidae may be a grade rather than a clade.

A supertree of temnospondyli: cladogenetic patterns in the most species-rich group of early tetrapods.

As the most diverse group of early tetrapods, temnospondyls provide a unique opportunity to investigate cladogenetic patterns among basal limbed vertebrates. We present five species-level supertrees for temnospondyls, built using a variety of methods. The standard MRP majority rule consensus including minority components shows slightly greater resolution than other supertrees, and its shape matches well several currently accepted hypotheses of higher-level phylogeny for temnospondyls as a whole. Also, its node support is higher than those of other supertrees (except the combined standard plus Purvis MRP supertree). We explore the distribution of significant as well as informative changes (shifts) in branch splitting employing the standard MRP supertree as a reference, and discuss the temporal distribution of changes in time-sliced, pruned trees derived from this supertree. Also, we analyse those shifts that are most relevant to the end-Permian mass extinction. For the Palaeozoic, shifts occur almost invariably along branches that connect major Palaeozoic groups. By contrast, shifts in the Mesozoic occur predominantly within major groups. Numerous shifts bracket narrowly the end-Permian extinction, indicating not only rapid recovery and extensive diversification of temnospondyls over a short time period after the extinction event (possibly less than half a million years), but also the role of intense cladogenesis in the late part of the Permian (although this was counteracted by numerous 'background' extinctions).

Biphasic Hoxd Gene Expression in Shark Paired Fins Reveals an Ancient Origin of the Distal Limb Domain

The evolutionary transition of fins to limbs involved development of a new suite of distal skeletal structures, the digits. During tetrapod limb development, genes at the 5′ end of the HoxD cluster are expressed in two spatiotemporally distinct phases. In the first phase, Hoxd9-13 are activated sequentially and form nested domains along the anteroposterior axis of the limb. This initial phase patterns the limb from its proximal limit to the middle of the forearm. Later in development, a second wave of transcription results in 5′ HoxD gene expression along the distal end of the limb bud, which regulates formation of digits. Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods. Here we test this hypothesis by investigating Hoxd gene expression during paired fin development in the shark Scyliorhinus canicula, a member of the most basal lineage of jawed vertebrates. We report that at early stages, 5′Hoxd genes are expressed in anteroposteriorly nested patterns, consistent with the initial wave of Hoxd transcription in teleost and tetrapod paired appendages. Unexpectedly, a second phase of expression occurs at later stages of shark fin development, in which Hoxd12 and Hoxd13 are re-expressed along the distal margin of the fin buds. This second phase is similar to that observed in tetrapod limbs. The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans. We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.

Devonian climate change, breathing, and the origin of the tetrapod stem group

The diversification of the tetrapod stem group occurred during the late Middle through the Late Devonian, that is from the Givetian to Famennian stages about 385-365 million years ago. The relationships between the known taxa representing this radiation have currently reached a reasonable consensus so that interpretations of the order of appearance of tetrapod characters is possible. The immediate fish relatives of the earliest limbed tetrapods show what is interpreted as a progressive increase in the spiracular chamber and its opening to the outside. Here, this is inferred to be associated with an increased capacity for air-breathing. Lungs are thought to have been present in most early bony fishes, and were most likely ventilated by air-gulping. This could have brought about a facultative capacity for air-breathing, which the tetrapod stem group exploited to the greatest degree. These adaptations are shown not only in freshwater forms but also in estuarine and marginal marine forms. Estimates of oxygen levels during this period suggest that they were unprecedentedly low during the Givetian and Frasnian periods. At the same time, plant diversification was at its most rapid, changing the character of the landscape and contributing, via soils, soluble nutrients, and decaying plant matter, to anoxia in all water systems. The co-occurrence of these global events may explain the evolution of air-breathing adaptations in at least two lobe-finned groups, contributing directly to the rise of the tetrapod stem group. In contrast to recent studies, low atmospheric oxygen is not considered to be a causal factor in the lack of fossils documenting the evolution of Early Carboniferous tetrapods.

Physiological and morphological responses to feeding in broad-nosed caiman (Caiman latirostris)

Broad nosed caiman are ectotherm sauropsids that naturally experience long fasting intervals. We have studied the postprandial responses by measuring oxygen consumption using respirometry, the size changes of the duodenum, the distal small intestine, and the liver, using repeated non-invasive ultrasonography, and by investigating structural changes on the level of tissues and cells by using light- and electron microscopy. The caimans showed the same rapid and reversible changes of organ size and identical histological features, down to the ultrastructure level, as previously described for other ectothermic sauropsids. We found a configuration change of the mucosa epithelium from pseudostratified during fasting to single layered during digestion, in association with hypertrophy of enterocytes by loading them with lipid droplets. Similar patterns were also found for the hepatocytes of the liver. By placing the results of our study in comparative relationship and by utilizing the phylogenetic bracket of crocodiles, birds and squamates, we suggest that the observed features are plesiomorphic characters of sauropsids. By extending the comparison to anurans, we suggest that morphological and physiological adjustments to feeding and fasting described here may have been a character of early tetrapods. In conclusion, we suggest that the ability to tolerate long fasting intervals and then swallow a single large meal as described for many sit-an-wait foraging sauropsids is a functional feature that was already present in ancestral tetrapods.

Re-Examination of Some Large Early Mesozoic Tetrapod Footprints from the African Collection of Paul Ellenberger

The Late Triassic—Early Jurassic ichnofauna described mainly by Paul Ellenberger from southern Africa (Lesotho) is a valuable window on first phases of dinosaur diversification. Unfortunately, the present taxonomic status of several forms from that ichnofauna is unclear. The revision of this material has been frequently invoked and partially done without reaching many definitive results. Due to the enormous amount of data, a global revision seems at present impossible and must be accomplished in smaller steps. A small number of Ellenberger's ichnogenera including Tetrasauropus, Pseudotetrasauropus, Pentasauropus, Paratetrasauropus, Sauropodopus and Deuterosauropodopus, which different authors have ascribed to basal sauropodomorphs, are here revised in a consistent manner and their attribution to osteological clades is considered. Tetrasauropus and Pseudotetrasauropus are here validated as the only ichnotaxa related to sauropodomorphs. Pentasauropus is retained as valid, and a therapsid trackmaker is suggested. Paratetrasauropus and Sauropodopus are also validated and ascribed to non-dinosaurian trackmakers, and Deuterosauropodopus is synonymized with Sauropodopus.

Terrestrial-style feeding in a very early aquatic tetrapod is supported by evidence from experimental analysis of suture morphology

There is no consensus on when in the fish-tetrapod transition suction feeding, the primary method of prey capture in the aquatic realm, evolved into the direct biting on prey typical of terrestrial animals. Here, we show that differences in the morphology of selected cranial sutures between species that span the fish-tetrapod transition (the Devonian osteolepiform fish Eusthenopteron, the aquatic Devonian tetrapod Acanthostega, and the Permian terrestrial tetrapod Phonerpeton) can be used to infer when terrestrial feeding first appeared. Our approach consists of defining a sutural morphospace, assigning functional fields to that morphospace based on our previous measurements of suture function made during feeding in the living fish Polypterus, inferring the functions of the fossil sutures based on where they fall in the morphospace, and then using the correlation between feeding mode and the patterns of inferred suture function across the skull roof in taxa where feeding mode is unambiguous to infer the feeding mode practiced by Acanthostega. Using this procedure, we find that the suture morphologies of Acanthostega are inconsistent with the hypothesis that it captured prey primarily by means of suction, which suggests that it may have bitten directly on prey at or near the water's edge. Thus, our data strongly support the hypothesis that the terrestrial mode of feeding first emerged in aquatic taxa.

The skull and the palaeoecological significance of Labidosaurus hamatus, a captorhinid reptile from the Lower Permian of Texas

The cranial skeleton of the large captorhinid reptile Labidosaurus hamatus, known only from the Lower Permian of Texas, is described on the basis of new, undescribed specimens. Labidosaurus is distinguished from other captorhinids by the more extreme sloping of the ventral (alveolar) margin of the premaxilla, a low dorsum sellae of the parabasisphenoid, a reduced prootic, a narrow stapes, and a relatively small foramen intermandibularis medius. Despite the presence of a single row of teeth in each jaw, the skull of Labidosaurus resembles most closely those of moradisaurines, the large multiple-tooth-rowed captorhinids of the latest Early and Middle Permian. A phylogenetic analysis confirms that the single-tooth-rowed L. hamatus is related most closely to moradisaurines within Captorhinidae, a relationship that supports the hypothesis of a diphyletic origin for multiple rows of marginal teeth in captorhinids (in the genus Captorhinus and in the clade Moradisaurinae). In view of the close relationship between L. hamatus and moradisaurines, which are regarded to have been herbivorous, L. hamatus is a critical taxon for studies of the evolution of herbivory in early tetrapods. L. hamatus shares several trademark features of herbivorous adaptation with moradisaurines, which suggest that this captorhinid species was omnivorous. As such, it represents a transitional taxon between faunivorous basal reptiles and the herbivorous moradisaurines. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 237–262.

Dates, nodes and character conflict: Addressing the Lissamphibian origin problem

Synopsis Extant amphibians consist of Salientia (frogs), Caudata (salamanders), and Gymnophiona (caecilians). The mutual relationships of these groups are controversial, with either Batrachia (Salientia + Caudata) or Procera (Gymnophiona + Caudata) as emerging clades in recent molecular and morphological analyses. The monophyly of amphibians as a whole is supported by independent data, but their origins and affinities with early tetrapods are debated. A new cladistic analysis of early tetrapods retrieves Temnospondyli (the most species‐rich group of early tetrapods) as the closest relatives of crown group amphibians. One temnospondyl group, the Dissorophoidea, forms a series of consecutive outgroups to crown amphibians. In particular, the Lower Permian amphibamid Doleserpeton is the most derived plesion on the amphibian stem. The Albanerpetontidae, a group of salamander‐like tetrapods ranging from the Jurassic to the Pliocene, are placed as stem Gymnophiona. The shortest trees support the Batrachia hypothesis. However, the Procera hypothesis is not a significantly worse fit for the whole character set. Exhaustive treatment of characters and taxa is the most appropriate way to disentangle contrasting phylogenetic signals in large matrices. Tests of different crown topologies show that placement of amphibians within lepospondyls (e.g. as sister taxon to Lysorophia) is not a significantly worse fit for the whole character set than a close temnospondyl‐lissamphibian relationship. However, the latter phylogenetic hypothesis best captures the most coherent assembly of derived lissamphibian apomorphies.

Visual pigments in a living fossil, the Australian lungfish Neoceratodus forsteri

BackgroundOne of the greatest challenges facing the early land vertebrates was the need to effectively interpret a terrestrial environment. Interpretation was based on ocular adaptations evolved for an aquatic environment millions of years earlier. The Australian lungfish Neoceratodus forsteri is thought to be the closest living relative to the first terrestrial vertebrate, and yet nothing is known about the visual pigments present in lungfish or the early tetrapods.ResultsHere we identify and characterise five visual pigments (rh1, rh2, lws, sws1 and sws2) expressed in the retina of N. forsteri. Phylogenetic analysis of the molecular evolution of lungfish and other vertebrate visual pigment genes indicates a closer relationship between lungfish and amphibian pigments than to pigments in teleost fishes. However, the relationship between lungfish, the coelacanth and tetrapods could not be absolutely determined from opsin phylogeny, supporting an unresolved trichotomy between the three groups.ConclusionThe presence of four cone pigments in Australian lungfish suggests that the earliest tetrapods would have had a colorful view of their terrestrial environment.

Evolution of sound localization in lizards

Tympanic hearing may have developed independently in four major tetrapod groups, the anurans, lepidosaurs, archosaurs, and mammals. The emergence of a tympanic ear would have increased the frequency range and sensitivity of hearing. Furthermore, early tympana were acoustically coupled through the mouth cavity and therefore must have acted as pressure difference receivers, which are inherently directional, obviating a need for central computation of ITD and ILD. In lizards, this acoustical coupling generates a large directional difference at the tympanum and recordings from auditory nerve are strongly ITD‐ and ILD‐dependent. To separate neural from acoustical interactions, interaural transmission in a gecko was blocked to reveal true binaural neurons in nucleus magnocellularis, nucleus angularis, and superior olive. The function of these neurons with naturalistic, i.e., free‐field stimulation may be to sharpen the directional response, a mechanism similar to that suggested for teleost fish. The closure of the middle ear cavity in the mammals and some birds is a derived condition, and may have profoundly changed the operation of the ancestral tetrapod ear by decoupling the tympana, improving the low‐frequency response of the tympanum, and leading to a requirement for neural computation of directionality in the central nervous system.

LATE DEVONIAN (FAMENNIAN) LUNGFISHES FROM THE CATSKILL FORMATION OF PENNSYLVANIA, USA

Abstract: Occurrences of fossil lungfishes (Dipnoi: Sarcopterygii) in the Famennian Catskill Formation of Pennsylvania are reviewed. A nearly complete dermal skull roof is assigned to a new genus and species, Apatorhynchus opistheretmus. Other recently discovered lungfish specimens include an incomplete postcranium similar to that of the Frasnian genus Fleurantia, a small parasphenoid of uncertain affinities, and isolated toothplates. Previously described dipnoan remains from the Catskill Formation include a partial skull roof of Soederberghia groenlandica, toothplates assigned to several species of Dipterus, a putative rostral or symphysial region placed in the problematic form taxon Ganorhynchus, and sedimentary structures interpreted as burrows. The toothplates attributed to Dipterus are indeterminate and are placed in open nomenclature, while the specimen identified as Ganorhynchus is not convincingly dipnoan. The status of the burrows remains uncertain pending the discovery of lungfish remains within these or similar structures in Catskill deposits. The distinct ichthyofaunas within the Catskill Formation and their lungfish components are briefly reviewed. Lungfishes are found in the Holoptychius‐ and Bothriolepis‐dominated faunas common in the Catskill succession, as well as in the compositionally distinctive Red Hill assemblage. Many of the Devonian continental faunas that contain tetrapods also include long‐snouted, denticle‐bearing lungfishes (‘rhynchodipterids’, fleurantiids, or both). The composition of Late Devonian ichthyofaunas may have predictive qualities that will allow researchers to identify localities likely to produce the remains of early tetrapods.

Biomechanics of the vertebrae and associated osteoderms of the Early Permian amphibian Cacops aspidephorus

AbstractTwo series of osteoderms associated with the anterior three‐quarters of the presacral vertebral column of the Early Permian temnospondylous amphibian Cacops aspidephorus have important implications for biomechanics of the axial skeleton. An internal series consists of an osteoderm fused to the distal tip of each neural spine. Lying dorsal to the internal series and overlapping each internal osteoderm is a second external series. The orientation of the zygapophyseal facets implies modest lateral flexion with limited coupled axial rotation of the column. However, the osteoderms restricted any possible lateral flexion through their inverted V‐shape, strongly angled overlap between each external osteoderm and its neighbouring internal osteoderms, and the presence of a midsagittal flange on the ventral surface of each external osteoderm that fits into grooves on the anterior and posterior edges of the neighbouring internal osteoderms. This configuration allowed vertical flexion of the vertebral column with little lateral flexion. The rod‐like nature of osteoderms with the anterior three‐quarters of the presacral vertebrae suggests a restricted form of forward movement for Cacops unlike that of other early tetrapods.

SIGOURNEA MULTIDENTATA, A NEW STEM TETRAPOD FROM THE UPPER MISSISSIPPIAN OF IOWA, USA

Sigournea multidentata n. gen. and sp., an early tetrapod, is described from the Late Mississippian Delta locality of southern Iowa, USA. The holotype and only known specimen, a right mandible, is unique in the structure of the symphysial region, and in addition has a unique combination of characters that are shared with other tetrapods. The free ventral border of the single exomeckelian fenestra is formed by infradentary bones. Its visible portion shows several arch bases, separated by notched or straight intervals. This morphology is interpreted as indicating that the arch bases and intervals between them reflected a series of Meckelian fenestrae that were partly exo- and partly endoskeletal, due to the fact that the exoskeletal arch bases continued dorsally in Meckelian cartilage. We suggest that this may exemplify a stage in the evolution of exomeckelian fenestrae, in at least some lineages of early tetrapods. The relations of Sigournea are indeterminate. That it is a tetrapod is indicated by the presence of pit and ridge ornamentation, an open lateral line sulcus, a dorsally directed glenoid, a single elongate exomeckelian fenestra, absence of intercoronoid fossae, absence of coronoid fangs, a single row of marginal teeth on the dentary, and an absence of dentition on the prearticular. It is at present impossible to determine its relationship with other early tetrapods, and we conclude that Sigournea is best considered as an early tetrapod incertae sedis.

Origin of dental occlusion in tetrapods: signal for terrestrial vertebrate evolution?

Evolutionary changes of the dentition in tetrapods can be associated with major events in the history of terrestrial vertebrates. Dental occlusion, the process by which teeth from the upper jaw come in contact with those in the lower jaw, appears first in the fossil record in amniotes and their close relatives near the Permo-Carboniferous boundary approximately 300 million years ago. This evolutionary innovation permitted a dramatic increase in the level of oral processing of food in these early tetrapods, and has been generally associated with herbivory. Whereas herbivory in extinct vertebrates is based on circumstantial evidence, dental occlusion provides direct evidence about feeding strategies because jaw movements can be reconstructed from the wear patterns of the teeth. Examination of the evolution of dental occlusion in Paleozoic tetrapods within a phylogenetic framework reveals that this innovation developed independently in several lineages of amniotes, and is represented by a wide range of dental and mandibular morphologies. Dental occlusion also developed within diadectomorphs, the sister taxon of amniotes. The independent, multiple acquisition of this feeding strategy represents an important signal in the evolution of complex terrestrial vertebrate communities, and the first steps in the profound changes in the pattern of trophic interactions in terrestrial ecosystems.

Tetrapod-like middle ear architecture in a Devonian fish

Few fossils show the incipient stages of complex morphological transformations. For example, the earliest stages in the remodelling of the spiracular tract and suspensorium (jaw suspension) of osteolepiform fishes into the middle ear of tetrapods have remained elusive. The most primitive known tetrapods show a middle ear architecture that is very different from osteolepiforms such as Eusthenopteron, with little indication of how this transformation took place. Here we present an analysis of tetrapod middle ear origins that is based on a detailed study of Panderichthys, the immediate sister taxon of tetrapods. We show that the spiracular region is radically transformed from osteolepiforms and represents the earliest stages in the origin of the tetrapod middle ear architecture. The posterior palatoquadrate of Panderichthys is completely tetrapod-like and defines a similarly tetrapod-like spiracular tract. The hyomandibula has lost its distal portion, representing a previously unrecognized advance towards a stapes-like morphology. This spiracular specialization suggests that the middle ear of early tetrapods evolved initially as part of a spiracular breathing apparatus.

Postcranial myology of the California newt, Taricha torosa

Salamanders are generally agreed to represent the primitive tetrapod body plan, as well as a postural analog for early tetrapods. Dissection and description of the muscles of the forelimb, trunk, and hindlimb of the California newt, Taricha torosa, were undertaken to provide baseline data on the locomotor structures in this species. Hypaxial trunk muscles are similar to those of other vertebrates. As in other salamanders, limb muscles show a simple parallel-fibered architecture and often span multiple joints. Several differences in limb musculature were also noted. The extensor iliotibialis muscle possesses a single head in T. torosa, rather than the two heads common in larger salamander species. The ischioflexorius muscle, while divided into proximal and distal sections, is not distinct from the puboischiotibialis in its proximal portion. The femorofibularis is enlarged in this species; it is suggested that the femorofibularis and ischioflexorius muscles may be functionally analogous systems. Forelimb and hindlimb musculature show similar morphological patterns, particularly in distal limb segments, which may provide insight into the primitive arrangement of tetrapod limb muscles.

The pelvic fin and girdle of Panderichthys and the origin of tetrapod locomotion

One of the most marked transformations in the vertebrate transition to land was that of fins to limbs. This transformation involved not only the generation of morphological novelties (digits, sacrum) but also a shift in locomotory dominance from the pectoral to the pelvic appendage. Despite its importance, the transformation from pelvic fin to hindlimb is the least studied and least well-documented part of this transformation, which is bracketed by the osteolepiform Eusthenopteron and the early tetrapods Ichthyostega and Acanthostega, but is not directly illuminated by any intermediate form. Panderichthys is the closest tetrapod relative currently represented by complete fossils, but its pelvic fin skeleton has not been described. Here, I present the only known articulated pelvic fin endoskeleton and associated partial pelvis of Panderichthys. The pelvic girdle is even less tetrapod-like than that of the osteolepiform Eusthenopteron, but the pelvic fin endoskeleton shares derived characteristics with basal tetrapods despite being more primitive than the pectoral fin of Panderichthys. The evolution of tetrapod locomotion appears to have passed through a stage of body-flexion propulsion, in which the pelvic fins played a relatively minor anchoring part, before the emergence of hindlimb-powered propulsion in the interval between Panderichthys and Acanthostega.

A gigantic fossil arthropod trackway

A unique, complex trackway has been discovered in Scotland: it was made roughly 330 million years ago by a huge, six-legged water scorpion that was about 1.6 m long and a metre wide. To my knowledge, this is not only the largest terrestrial trackway of a walking arthropod to be found so far, but is also the first record of locomotion on land for a species of Hibbertopterus (Eurypterida). This evidence of lumbering movement indicates that these giant arthropods, now extinct, could survive out of water at a time when the earliest tetrapods were making their transition to the land.

The emergence of early tetrapods

Study of Devonian tetrapods and their relatives spanning the so-called ‘fish–tetrapod’ transition has expanded almost exponentially in the last 15 years or so. This evolutionary event is now represented by at least nine named genera of Devonian tetrapod, several new ‘near-tetrapods’ and a number of new tetrapods from the Early Carboniferous. The anatomy of Acanthostega has radically changed ideas about how this transition took place, and more recently the anatomy of Ichthyostega is being reassessed with some startling conclusions such as the unique construction of its ear region. The current state of research on this range of animals is summarized, followed by a consideration of the acquisition of limbs and digits among tetrapods including their possible forerunners, the development of digits and their original function, and the onset of pentadactyly. The faunal relations and palaeoecological contexts of the Devonian tetrapods are brought together in an initial though necessarily brief survey, followed by an assessment of Devonian tetrapod diversity, which is seen to be much greater than previously realised. Finally, some hopes and ambitions for the future are set out.