Stem Amniotes Research Articles

The Evolution of Transglutaminases Underlies the Origin and Loss of Cornified Skin Appendages in Vertebrates.

Transglutaminases (TGMs) cross-link proteins by introducing covalent bonds between glutamine and lysine residues. These cross-links are essential for epithelial cornification which enables tetrapods to live on land. Here, we investigated which evolutionary adaptations of vertebrates were associated with specific changes in the family of TGM genes. We determined the catalog of TGMs in the main clades of vertebrates, performed a comprehensive phylogenetic analysis of TGMs, and localized the distribution of selected TGMs in tissues. Our data suggest that TGM1 is the phylogenetically oldest epithelial TGM, with orthologs being expressed in the cornified teeth of the lamprey, a basal vertebrate. Gene duplications led to the origin of TGM10 in stem vertebrates, the origin of TGM2 in jawed vertebrates, and an increasing number of epithelium-associated TGM genes in the lineage leading to terrestrial vertebrates. TGM9 is expressed in the epithelial egg tooth, and its evolutionary origin in stem amniotes coincided with the evolution of embryonic development in eggs that are surrounded by a protective shell. Conversely, viviparous mammals have lost both the epithelial egg tooth and TGM9. TGM3 and TGM6 evolved as regulators of cornification in hair follicles and underwent pseudogenization upon the evolutionary loss of hair in cetaceans. Taken together, this study reveals the gain and loss of vertebrate TGM genes in association with the evolution of cornified skin appendages and suggests an important role of TGM9 in the evolution of amniotes.

A diadectid skin impression and its implications for the evolutionary origin of epidermal scales.

Corneous skin appendages are not only common and diverse in crown-group amniotes but also present in some modern amphibians. This raises the still unresolved question of whether the ability to form corneous skin appendages is an apomorphy of a common ancestor of amphibians and amniotes or evolved independently in both groups. So far, there is no palaeontological contribution to the issue owing to the lack of keratin soft tissue preservation in Palaeozoic anamniotes. New data are provided by a recently discovered ichnofossil specimen from the early Permian of Poland that shows monospecific tetrapod footprints associated with a partial scaly body impression. The traces can be unambiguously attributed to diadectids and are interpreted as the globally first evidence of horned scales in tetrapods close to the origin of amniotes. Taking hitherto little-noticed scaly skin impressions of lepospondyl stem amniotes from the early Permian of Germany into account, the possibility has to be considered that the evolutionary origin of epidermal scales deeply roots among anamniotes.

Problems of the interrelationships of crown and stem amniotes

Amniota is a tetrapod group that was recognized originally in the 19th century on the basis of developmental features (extra-embryonic membranes), but since the widespread adoption of phylogenetic systematics in the late 20th century, it has been recast as a crown clade. The oldest amniotes are Late Carboniferous in age (ca. 318 million years ago), and they are preserved in coal beds and lycopod tree stumps that have yielded rich faunas of temnospondyls, anthracosaurs, and other early tetrapods. Numerous phylogenetic studies of the past three decades have focused on the relationships of amniotes to other early tetrapods, resulting in the prevailing picture that Amniota is the crown of a total group with many extinct Paleozoic clades comprising its stem group. The content and the sequence of branching among stem amniotes are vigorously debated topics in early tetrapod paleontology. The ‘traditional’ stem amniote group Diadectomorpha has been proposed as the sister group of synapsid amniotes in a series of papers by one research group. If correct, the placement of Diadectomorpha within Amniota implies that high-fiber herbivory, a key component of terrestrial vertebrate ecosystems of modern aspect, is an entirely amniote phenomenon. Another stem group, Recumbirostra, has been recovered by other researchers within Amniota as reptiles. Recumbirostrans exhibit cranial features that are correlated with a fossorial lifestyle, and most species for which we have postcrania reveal the phenomena of body elongation and many of these exhibit limb reduction. If correct, the identification of recumbirostrans as early reptiles not only greatly augments the content of Paleozoic Amniota but also marks the evolution of skeletal features indicative of a burrowing lifestyle that predates the appearance of unequivocal fossorial amniotes (cistecephalid dicynodonts) by 40 million years. However, it is premature to accept either diadectomorphs or recumbirostrans as amniotes, given issues with scorings for amniote taxa, character argumentation, and poor homologization of braincase features between amniote and anamniote taxa.

Recumbirostran ‘microsaurs’ are not amniotes

Amniota is a tetrapod clade that includes extant mammals and reptiles, including birds, as well as a wealth of extinct taxa extending over 318 million years of Earth’s history. For over three decades, Amniota has been treated as a crown group, but the content of stem amniotes has varied among large-scale analyses of Palaeozoic tetrapods. Nine recent phylogenetic studies on Palaeozoic tetrapods, all derived from each other, have potentially changed our perspectives on amniote origins and early evolution. The first of these analyses posited that two particular clades of Palaeozoic tetrapods, Recumbirostra and Lysorophia, both previously considered to be lepospondyl stem-amniotes, are actually amniotes. This raises the possibility that early amniotes included both small fossorial and terrestrial animals, some of which show strong evidence of limb reduction. Here we show that the strange position of these small, often fossorial and limb-reduced tetrapods in Amniota is the result of two fundamental flaws: (1) the phylogenetic analysis combines two separate data matrices that were each designed to test only patterns of relationships among early anamniote tetrapods; and (2) the absence of key amniote characters. Our reanalysis of Palaeozoic tetrapod interrelationships reinstates recumbirostrans and lysorophians outside Amniota. The results of our study impact other recent studies that have simply accepted the codings in the data matrix that resulted in the hypothesis that recumbirostrans are amniotes and raises important questions about the initial diversification of amniotes and the evolution of fossoriality and limb reduction among tetrapods.

Neurosensory anatomy and function in Seymouria.

Seymouria is among the best-known stem amniotes and holds an important phylogenetic position for discussions of amniote evolution. Previous work has focused primarily on the osteology of Seymouria, with recent interest turning to the application of computed tomography (CT) to study the internal features. We utilized neutron CT to reconstruct the first virtual cranial endocast and the first complete otic endocasts of Seymouria, revealing previously unrecognized details of its palaeoneuroanatomy. The brain and inner ear of Seymouria are largely plesiomorphic relative to later-diverging crown amniotes, showing no indication of increased encephalization or braincase ossification. Our results also clarify the plesiomorphic condition for carotid artery morphology in amniotes, with Seymouria showing a similar condition to basal members of both the synapsid and sauropsid lineages. The reconstructed neuroanatomy also indicates that Seymouria did not possess any particular neuroanatomical specializations, despite the probable presence of an impedance matching hearing system. This article is protected by copyright. All rights reserved.

Dental anatomy and replacement patterns in the early Permian stem amniote, Seymouria.

The exquisite preservation of maxillary and mandibular fragments of Seymouria has allowed us to examine for the first time in detail the dental anatomy and patterns of development in this stem amniote. The results obtained through histological examination show that Seymouria has pleurodont implantation with ankylosis of the tooth to the labial side of the jawbone. The dentary and maxillary teeth exhibit similar dental characteristics, such as the attachment bone (alveolar bone) and cementum rising above the jawbone on the base of the tooth, and smooth carinae extending lingually toward the tooth apex. Additionally, the clear presence of plicidentine, infolding of dentine into the pulp cavity, was found within the tooth root extending into the tooth crown. Lastly, the tooth replacement pattern is alternating, illustrating that Seymouria retains the classic primitive condition for tetrapods, a pattern that is continued in amniotes. Our results provide an important basis for comparison with other stem amniotes and with amniotes.

A Mississippian (early Carboniferous) tetrapod showing early diversification of the hindlimbs

The taxonomically diverse terrestrial tetrapod fauna from the late Mississippian East Kirkton Limestone includes the earliest known members of stem Amphibia and stem Amniota. Here we name and describe a new East Kirkton tetrapod with an unusual hindlimb morphology reminiscent of that of several stem- and primitive crown amniotes. It displays a unique ilium with two slender and elongate processes and a 5-digit pes with a long, stout metatarsal IV and a greatly elongate digit IV. The new taxon broadens our knowledge of East Kirkton tetrapods, adding to the remarkable diversity of their hindlimb constructions, functional specializations, locomotory modes, and adaptations to a wide variety of substrates. An unweighted character parsimony analysis places the new taxon in a polytomy alongside some other Carboniferous groups. Conversely, weighted parsimony and Bayesian analyses retrieve it among the earliest diverging stem amniotes, either as the basalmost anthracosaur or within a clade that includes also Eldeceeon and Silvanerpeton, crownward of an array of chroniosaurs plus anthracosaurs.

Modeling Sprawling Locomotion of the Stem Amniote Orobates: An Examination of Hindlimb Muscle Strains and Validation Using Extant Caiman

The stem amnioteOrobates pabstihas been reconstructed to be capable of relatively erect, balanced, and mechanically power-saving terrestrial locomotion. This suggested that the evolution of such advanced locomotor capabilities preceded the origin of crown-group amniotes. We here further investigate plausible body postures and locomotion ofOrobatesby taking soft tissues into account. Freely available animation software BLENDERis used to first reconstruct the lines of action of hindlimb adductors and retractors forOrobatesand then estimate the muscle strain of these muscles. We experimentally varied different body heights in modeled hindlimb stride cycles ofOrobatesto find the posture that maximizes optimal strains over the course of a stride cycle. To validate our method, we usedCaiman crocodilus. We replicated the identical workflow used for the analysis ofOrobatesand compared the locomotor posture predicted forCaimanbased on muscle strain analysis with this species’ actual postural data known from a previously published X-ray motion analysis. Since this validation experiment demonstrated a close match between the modeled posture that maximizes optimal adductor and retractor muscle strain and thein vivoposture employed byCaiman, using the same method forOrobateswas justified. Generally, the use of muscle strain analysis for the reconstruction of posture in quadrupedal vertebrate fossils thus appears a promising approach. Nevertheless, results forOrobatesremained inconclusive as several postures resulted in similar muscle strains and none of the postures could be entirely excluded. These results are not in conflict with the previously inferred moderately erect locomotor posture ofOrobatesand suggest considerable variability of posture during locomotion.

A review of the stem amnioteEldeceeon rolfeifrom the Viséan of East Kirkton, Scotland

ABSTRACTThe late Viséan anthracosauroidEldeceeon rolfeifrom the East Kirkton Limestone of Scotland is re-described. Information from two originally described and two newly identified specimens broadens our knowledge of this tetrapod. A detailed account of individual skull bones and a revision of key axial and appendicular features are provided, alongside the first complete reconstructions of the skull and lower jaw and a revised reconstruction of the postcranial skeleton. In comparison toSilvanerpeton, the only other anthracosauroid from East Kirkton,Eldeceeonis characterised by a proportionally wider semi-elliptical skull, comparatively smaller nostrils set farther apart, smaller and more rounded orbits, a shorter skull table with gently convex lateral margins, and a deeper suspensorium with a straight posterior margin and a small dorsal embayment. The remarkably large hind feet and elongate toes ofEldeceeonpresumably represent an adaptation for attaining high locomotory speed through increased stride length and reduced stride frequency. This would necessitate great muscle force but few muscle contractions. At the beginning of a new stride cycle, repositioning the pes anteriorly and lifting the toes off the ground would require a strong and large muscle to pull the femur upward and rotate it inward and forward. It is hypothesised that such muscle might correspond to thepuboischiofemoralis internus 2, which would extend along the posterior half of the vertebral column, consistent with the occurrence of long, curved ribs in the anterior half of the trunk. Using maximum parsimony and Bayesian inference, cladistic analyses of all major groups of stem amniotes retrieve a sister group relationship betweenEldeceeonandSilvanerpeton, either as the most plesiomorphic stem amniote clade or as a clade immediately crownward of anthracosauroids.

Locomotor rib kinematics in two species of lizards and a new hypothesis for the evolution of aspiration breathing in amniotes

Most lizards walk and run with a sprawling gait in which the limbs are partly advanced by lateral undulation of the axial skeleton. Ribs and vertebrae are integral to this locomotor mode, but 3D motion of the axial skeleton has not been reported for lizard locomotion. Here, we use XROMM to quantify the relative motions of the vertebrae and ribs during slow treadmill locomotion in three savannah monitor lizards (Varanus exanthematicus) and three Argentine black and white tegus (Salvator merianae). To isolate locomotion, we selected strides with no concurrent lung ventilation. Rib rotations can be decomposed into bucket-handle rotation around a dorsoventral axis, pump-handle rotation around a mediolateral axis, and caliper rotations around a craniocaudal axis. During locomotion, every rib measured in both species rotated substantially around its costovertebral joint (8–17 degrees, summed across bucket, pump and caliper rotations). In all individuals from both species, the middle ribs rotated cranially through bucket and pump-handle motion during the propulsive phase of the ipsilateral forelimb. Axial kinematics during swing phase of the ipsilateral forelimb were mirror images of the propulsive phase. Although further work is needed to establish what causes these rib motions, active contraction of the hypaxial musculature may be at least partly responsible. Unilateral locomotor rib movements are remarkably similar to the bilateral pattern used for lung ventilation, suggesting a new hypothesis that rib motion during locomotion may have been an exaptation for the evolution of costal aspiration breathing in stem amniotes.

Limb-Bone Development of Seymouriamorphs: Implications for the Evolution of Growth Strategy in Stem Amniotes

Tetrapod life on land was the result of a lengthy process, the final steps of which resulted in full independence of amniotic tetrapods from the aquatic environment. Developmental strategies, including growth rate and the attainment of sexual maturity, played a major role in this transition. Early amniotes, such as Ophiacodon, tended to reach sexual maturity in a year while most non-amniotic Paleozoic tetrapods (including Devonian tetrapods and temnospondyls) became adult after 3 to 11 years. This ontogenetic transition is accompanied by a drastic change in growth rate and bone microstructure suggesting faster growth dynamics in early amniotes than in Devonian tetrapods and temnospondyls. Was the acquisition of a faster development (earlier sexual maturity and faster growth rate) a drastic evolutionary event or an extended process over geological time? To answer this question, the limb bone histology of two Early Permian (i.e. 270-290 million-year-old) stem-amniote seymouriamorphs, Seymouria sanjuanensis and Discosauriscus austriacus, were investigated. We used three-dimensional bone paleohistology based on propagation phase-contrast synchrotron microtomography. Both seymouriamorphs display relatively fast bone growth and dynamics (even though cyclic in the humerus of D. austriacus). This significantly contrasts with the slow primary bone deposition encountered in the stylopods of temnospondyls and Devonian (i.e. 360 million-year-old) stem tetrapods of similar sizes. On the basis of skeletochronological data, the seymouriamorph D. austriacus retained a long pre-reproductive period as observed in Devonian tetrapods and most temnospondyls. The combination of characteristics (faster growth rate but long pre-reproductive period) suggests that the shift towards an amniotic developmental strategy was an extended process in the evolutionary history of amniotes.

Postcranial anatomy and histology of Seymouria, and the terrestriality of seymouriamorphs.

Seymouria is the best known of the seymouriamorphs, a group of Permo-Carboniferous reptiliomorphs with both terrestrial and aquatic taxa. The majority of research on Seymouria has focused on cranial anatomy, with few detailed descriptions or illustrations of the postcrania. We utilized neutron computed tomography (nCT) and histological sampling to provide updated, detailed figures that clarify details of the postcranial anatomy and to assess the development and histology of Seymouria through specimens from the early Permian Richards Spur locality. The correlation of morphological and histological data indicate rapid metamorphosis in this terrestrially capable stem amniote, with the youngest specimen being postmetamorphic despite being distinctly younger than premetamorphic individuals of Discosauriscus, the only other seymouriamorph to have been histologically sampled. The microanatomical data (e.g., semi-open medullary cavity) also substantiate the hypothesis that Seymouria was terrestrial based on interpretation of external features, although the persistence of a modestly developed medullary spongiosa in comparison to either Discosauriscus or to other co-occurring terrestrial tetrapods suggests additional nuances that require further exploration. In the absence of clearly recognizable postmetamorphic stages in several seymouriamorph taxa, it is difficult to determine the evolutionary trajectory of terrestriality within the clade. Our analysis provides the first histological characterization of the life history of Seymouria and highlights the need for further study of seymouriamorph ontogeny.

New embolomerous tetrapod material and a faunal overview of the Mississippian-aged Point Edward locality, Nova Scotia, Canada

Embolomerous tetrapods, moderately-sized to large aquatic predators, form a major faunal constituent of Permo-Carboniferous tetrapod communities. Embolomeres are recognized by their distinct circular, bipartite vertebrae. Although traditionally classified as stem amniotes, the inclusion of embolomeres within the tetrapod crown group has recently been challenged. Despite the group’s phylogenetic uncertainty, embolomeres provide an important record of a long-lived tetrapod lineage, spanning “Romer’s Gap” through to the early Permian. Here, we describe embolomerous tetrapod material that was collected in 1915 by W.A. Bell (CMN 10015, herein divided into CMN 10015A, 10015B, and 10015C). The material, composed of numerous disarticulated cranial and postcranial elements, was discovered near Sydney, Nova Scotia, Canada, as ex situ beach-float pertaining to a horizon within the Mississippian-aged Point Edward Formation. Among this material, a single left lower jaw of a proterogyrinid is identified, differing from previous embolomere remains from this site identified as Pholiderpeton(?) bretonensis Romer, 1958. We also identify an anterior jaw fragment as a separate taxon from the proterogyrinid, indicating the presence of at least two embolomerous tetrapods in Bell’s collection. Other cranial and postcranial material cannot be directly associated with either jaw and are not diagnostic enough to assign to a specific taxon. Thus, the remaining material is referred to Embolomeri indet. until more information is available. Additionally, we summarize the fauna of the Point Edward locality revealing a diverse aquatic Late Mississippian ecosystem. Finally, the extensive embolomere material described here presents new data that can broadly address embolomere diversity throughout the Carboniferous.

First record of the stem amniote Discosauriscus (Seymouriamorpha, Discosauriscidae) from the Krkonoše Piedmont Basin (the Czech Republic)

The first record of the seymouriamorph stem amniote Discosauriscus from the Krkonoše Piedmont Basin (the Czech Republic) is described. The specimen is identified as D. pulcherrimus on the basis of the following features which are absent in D. austriacus: 1) the pointed tip of the ventrolateral process of the postorbital lies anteriorly to the tip of the wedge-shaped dorsomedial process of the jugal; and 2) the rows of small denticles diverge anteromedially and anterolaterally from the midwidth of the ventral surface of the palatal ramus of the pterygoid. This new record increases our knowledge of the occurrence of this seymouriamorph in the Permo-Carboniferous basins of Europe.

Reverse-engineering the locomotion of a stem amniote.

Reconstructing the locomotion of extinct vertebrates offers insights into their palaeobiology and helps to conceptualize major transitions in vertebrate evolution1-4. However, estimating the locomotor behaviour of a fossil species remains a challenge because of the limited information preserved and the lack of a direct correspondence between form and function5,6. The evolution of advanced locomotion on land-that is, locomotion that is more erect, balanced and mechanically power-saving than is assumed of anamniote early tetrapods-has previously been linked to the terrestrialization and diversification of amniote lineages7. To our knowledge, no reconstructions of the locomotor characteristics of stem amniotes based on multiple quantitative methods have previously been attempted: previous methods have relied on anatomical features alone, ambiguous locomotor information preserved in ichnofossils or unspecific modelling of locomotor dynamics. Here we quantitatively examine plausible gaits of the stem amniote Orobates pabsti, a species that is known from a complete body fossil preserved in association with trackways8. We reconstruct likely gaits that match the footprints, and investigate whether Orobates exhibited locomotor characteristics that have previously been linked to the diversification of crown amniotes. Our integrative methodology uses constraints derived from biomechanically relevant metrics, which also apply to extant tetrapods. The framework uses in vivo assessment of locomotor mechanics in four extant species to guide an anatomically informed kinematic simulation of Orobates, as well as dynamic simulations and robotics to filter the parameter space for plausible gaits. The approach was validated using two extant species that have different morphologies, gaits and footprints. Our metrics indicate that Orobates exhibited more advanced locomotion than has previously been assumed for earlier tetrapods7,9, which suggests that advanced terrestrial locomotion preceded the diversification of crown amniotes. We provide an accompanying website for the exploration of the filters that constrain our simulations, which will allow revision of our approach using new data, assumptions or methods.

Functional MRI in the Nile crocodile: a new avenue for evolutionary neurobiology.

Crocodilians are important for understanding the evolutionary history of amniote neural systems as they are the nearest extant relatives of modern birds and share a stem amniote ancestor with mammals. Although the crocodilian brain has been investigated anatomically, functional studies are rare. Here, we employed functional magnetic resonance imaging (fMRI), never tested in poikilotherms, to investigate crocodilian telencephalic sensory processing. Juvenile Crocodylus niloticus were placed in a 7 T MRI scanner to record blood oxygenation level-dependent (BOLD) signal changes during the presentation of visual and auditory stimuli. Visual stimulation increased BOLD signals in rostral to mid-caudal portions of the dorso-lateral anterior dorsal ventricular ridge (ADVR). Simple auditory stimuli led to signal increase in the rostromedial and caudocentral ADVR. These activation patterns are in line with previously described projection fields of diencephalic sensory fibres. Furthermore, complex auditory stimuli activated additional regions of the caudomedial ADVR. The recruitment of these additional, presumably higher-order, sensory areas reflects observations made in birds and mammals. Our results indicate that structural and functional aspects of sensory processing have been likely conserved during the evolution of sauropsids. In addition, our study shows that fMRI can be used to investigate neural processing in poikilotherms, providing a new avenue for neurobiological research in these critical species.

The evolution of cortical development: the synapsid-diapsid divergence.

The cerebral cortex covers the rostral part of the brain and, in higher mammals and particularly humans, plays a key role in cognition and consciousness. It is populated with neuronal cell bodies distributed in radially organized layers. Understanding the common and lineage-specific molecular mechanisms that orchestrate cortical development and evolution are key issues in neurobiology. During evolution, the cortex appeared in stem amniotes and evolved divergently in two main branches of the phylogenetic tree: the synapsids (which led to present day mammals) and the diapsids (reptiles and birds). Comparative studies in organisms that belong to those two branches have identified some common principles of cortical development and organization that are possibly inherited from stem amniotes and regulated by similar molecular mechanisms. These comparisons have also highlighted certain essential features of mammalian cortices that are absent or different in diapsids and that probably evolved after the synapsid-diapsid divergence. Chief among these is the size and multi-laminar organization of the mammalian cortex, and the propensity to increase its area by folding. Here, I review recent data on cortical neurogenesis, neuronal migration and cortical layer formation and folding in this evolutionary perspective, and highlight important unanswered questions for future investigation.

Skull and postcranium of the bystrowianid Bystrowiella schumanni from the Middle Triassic of Germany, and the position of chroniosuchians within Tetrapoda

Chroniosuchians form a mainly terrestrial or semi-terrestrial clade of Permian and Triassic crocodile- or varanid-like tetrapods, usually considered stem amniotes, but with disputed affinities within that grade. Two groups can be distinguished, the chroniosuchids and bystrowianids. Whereas the chroniosuchid skull and postcranium are well known, our knowledge of bystrowianids is restricted mainly to isolated vertebrae and osteoderms. The Middle Triassic bystrowianid Bystrowiella schumanni from south-western Germany was identified as the first taxon of this clade outside Russia and China, based on the morphology of its vertebrae and osteoderms. Here we expand on a full description of cranial and postcranial remains from this taxon, based on a partially articulated specimen and further isolated material. The material comprises large parts of the dermal skull roof, the pectoral girdle, ribs and limbs, and sheds light on many anatomical regions formerly unknown in bystrowianids. Among the autapomorphic features of Bystrowiella are the premaxilla with an edentulous crest lateral to the choana, the premaxillary teeth with conspicuous size differences, the jugal with an extremely long, narrow anterior process, and the enlarged postparietals and tabulars forming facets for articulation with the anteriormost osteoderm. As in chroniosuchids, the pre- and postfrontal are not in contact, but unlike in chroniosuchids, the internarial fontanelle and the antorbital fenestra are absent. In the amniote-like postcranium, the interclavicle is slender and has a conspicuous parasternal process, the humerus is waisted and bears a short supinator process, and the long, curved trunk ribs have widely separated rib heads and a slender shaft without blades or processes. Phylogenetic analysis, particularly based on numerous new postcranial features, supports the monophyly of chroniosuchians, even when the constituent synapomorphies (osteoderm and vertebral characters) are excluded from the matrix. Chroniosuchians nest at the base of the amniote stem, forming an unresolved polytomy with Silvanerpeton, embolomeres and more advanced stem amniotes.

The palatal dentition of tetrapods and its functional significance.

The presence of a palatal dentition is generally considered to be the primitive condition in amniotes, with each major lineage showing a tendency toward reduction. This study highlights the variation in palatal tooth arrangements and reveals clear trends within the evolutionary history of tetrapods. Major changes occurred in the transition between early tetrapods and amphibians on the one hand, and stem amniotes on the other. These changes reflect the function of the palatal dentition, which can play an important role in holding and manipulating food during feeding. Differences in the arrangement of palatal teeth, and in their pattern of loss, likely reflect differences in feeding strategy but also changes in the arrangement of cranial soft tissues, as the palatal dentition works best with a well-developed mobile tongue. It is difficult to explain the loss of palatal teeth in terms of any single factor, but palatal tooth patterns have the potential to provide new information on diet and feeding strategy in extinct taxa.

CO2-metabolism in early tetrapods revisited: inferences from osteological correlates of gills, skin and lung ventilation in the fossil record

One of the most important physiological changes during the conquest of land by vertebrates was the increasing reliance on lung breathing, with the concomitant decrease in importance of gill breathing. The main problem involved here was to cope with the excessive accumulation of CO2 in the body and to avoid respiratory acidosis. In the past, several often mutually contradicting hypotheses of CO2-elimination via skin, lungs and gills in early tetrapods have been proposed, based on theoretical physiological considerations and comparison with extant air-breathing fishes and amphibians. This study proposes a revised scenario of CO2-elimination in early tetrapods based on fossil evidence, that is recently identified osteological correlates of gills, skin structure and mode of lung ventilation. In stem tetrapods of the Devonian and Carboniferous, O2-uptake via the lungs by buccal pumping was decoupled from CO2-release via internal gills, and the rather gas-impermeable skin played a minor role in gaseous exchange. The two main lineages of crown-group tetrapods, the amphibian and amniote lineage, used different strategies of CO2-elimination. As in stem tetrapods, O2-uptake and CO2-release remained always largely decoupled in temnospondyls, which ventilated their lungs via buccal pumping and relied mainly on their internal gills for CO2-release. Temnospondyls were not able to reduce their internal gills before their skin became more gas permeable and their body size was reduced, to shift from internal gills to the skin as the major site of CO2-elimination, a pattern that is retained in most lissamphibians. In contrast, internal gills were lost very early in stem amniote evolution. This was associated with the evolution of the more effective aspiration pump that allowed the elimination of the bulk of CO2 via the lungs, leading to a coupled O2-uptake and CO2-loss in stem amniotes and later in amniotes.