Palaeozoic Tetrapods Research Articles

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.

Triassic stem caecilian supports dissorophoid origin of living amphibians

Living amphibians (Lissamphibia) include frogs and salamanders (Batrachia) and the limbless worm-like caecilians (Gymnophiona). The estimated Palaeozoic era gymnophionan–batrachian molecular divergence1 suggests a major gap in the record of crown lissamphibians prior to their earliest fossil occurrences in the Triassic period2–6. Recent studies find a monophyletic Batrachia within dissorophoid temnospondyls7–10, but the absence of pre-Jurassic period caecilian fossils11,12 has made their relationships to batrachians and affinities to Palaeozoic tetrapods controversial1,8,13,14. Here we report the geologically oldest stem caecilian—a crown lissamphibian from the Late Triassic epoch of Arizona, USA—extending the caecilian record by around 35 million years. These fossils illuminate the tempo and mode of early caecilian morphological and functional evolution, demonstrating a delayed acquisition of musculoskeletal features associated with fossoriality in living caecilians, including the dual jaw closure mechanism15,16, reduced orbits17 and the tentacular organ18. The provenance of these fossils suggests a Pangaean equatorial origin for caecilians, implying that living caecilian biogeography reflects conserved aspects of caecilian function and physiology19, in combination with vicariance patterns driven by plate tectonics20. These fossils reveal a combination of features that is unique to caecilians alongside features that are shared with batrachian and dissorophoid temnospondyls, providing new and compelling evidence supporting a single origin of living amphibians within dissorophoid temnospondyls.

Computed tomographic analysis of the cranium of the early Permian recumbirostran ‘microsaur’ Euryodus dalyae reveals new details of the braincase and mandible

AbstractRecumbirostran ‘microsaurs’ are a clade of Palaeozoic tetrapods that possess numerous morphological adaptations for fossorial ecologies. Re‐study of many ‘microsaurs’ using tomographic methods has provided substantial new data on poorly known anatomy that informs their debated phylogenetic position. Recent studies have identified suites of features among recumbirostrans that place the group within crown Amniota, contrary to hypothesized positions on the amniote stem or the lissamphibian stem. Herein we describe the cranial anatomy of the early Permian gymnarthrid Euryodus dalyae through tomographic analysis of the holotype from South Grandfield, Oklahoma and new specimens from karst deposits near Richards Spur. The braincase of E. dalyae is composed of well‐ossified pleurosphenoids, orbitosphenoids that brace against the skull roof, and unpaired median ossifications. The otic capsules are well‐ossified, and the occiput is unconsolidated. Analysis of the mandibles, typically obscured in articulated specimens, reveals a second tooth row on the dentary, a feature previously unknown in ‘microsaurs’ that is reminiscent of the condition of the co‐occurring captorhinid Captorhinus aguti. The Richards Spur specimens share many of these features, including the second tooth row, but the neurocranium of the scanned specimen (OMNH 53519) differs from that of the holotype of E. dalyae (e.g. absence of unpaired median ossifications), and these specimens are referred to Euryodus sp. These data add to the growing neurocranial dataset of ‘microsaurs’, which is essential for iterative reevaluation of early tetrapod phylogeny. This discovery of multiple tooth rows in ‘microsaurs’ provides further support for the hypothesized close relationships between ‘microsaurs’ and reptiles.

A new varanopid synapsid from the early Permian of Oklahoma and the evolutionary stasis in this clade.

Varanopids are a basal clade of small- to medium-sized non-therapsid synapsids, whose range extends from the late Pennsylvanian to the late middle Permian, and are found in North America, Russia, Europe and South Africa. The greatest varanopid diversity is observed at the fossiliferous cave deposits near Richards Spur, Oklahoma, well known for the preservation of a complex early Permian upland community. Two previously described varanopids, Mycterosaurus and Varanops, are known only from fragmentary disarticulated material at Richards Spur. A third putative varanopid, Basicranodon fortsillensis, represented by a partial parasphenoid, has been synonymized with Mycterosaurus longiceps. This study reports on a new varanopid taxon, represented by substantially more complete material, including three nearly complete skulls. Such comprehensive cranial material allows for a detailed study of the taxon and its relationship to other varanopids. This new varanopid bears great morphological similarity to Mesenosaurus romeri from the middle Permian Mezen River Basin of northern Russia. Phylogenetic analysis recovers a sister relationship between this taxon and Me. romeri. This relationship, in conjunction with a detailed morphological comparison, supports the placement of this taxon within Mesenosaurus, as a new species, Me. efremovi. These results reveal an unexpected extension of the geographical and temporal range of Mesenosaurus, contributing to our understanding of varanopid dispersal. The extended persistence of this basal clade of predatory synapsids, underscored by the apparent evolutionary stasis of this genus, is unusual among Palaeozoic tetrapods. This phenomenon implies an exceptionally high degree of extended ecological resilience across major faunal and environmental transitions.

The Definition of Bioregions in Palaeontological Studies of Diversity and Biogeography Affects Interpretations: Palaeozoic Tetrapods as a Case Study

Studies of diversity, whether of species richness within regions (alpha diversity) or faunal turnover between regions (beta diversity), will depend heavily on the “bioregions” into which a study area is divided. However, such studies in the palaeontological literature have often been extremely arbitrary in their definition of bioregions and have employed a wide variety of spatial scales, from individual localities to formations/basins to entire continents. Such bioregions will not necessarily be separated by biologically meaningful boundaries, and results obtained at different spatial scales will not be directly comparable. In many neontological studies, however, bioregions are defined more rigorously, usually as areas of endemicity. Here a procedure is proposed whereby this principal may be applied to palaeontological datasets. In each time bin/assemblage localities are subjected to two hierarchical cluster analyses, the first grouping the localities by geographic distance, the second by taxonomic distance. Clusters shared between the two will represent continuous geographic areas of endemicity and so may be used as bioregions. When calculating alpha or beta diversity through time, the spatial scale at which the bioregions are defined needs to be standardised between each time bin. This is done by grouping clusters of localities below a predefined geographic cluster node height. This approach is used to assess changes in beta diversity of Palaeozoic tetrapods and resolve disagreements regarding changes in faunal provinciality across the Carboniferous/Permian boundary. When the bioregions are defined at a smaller spatial scale, splitting the globe into many small regions, beta diversity decreases substantially during the earliest Permian. However, when the bioregions are defined at larger spatial scales, representing areas roughly the size of continents, beta diversity remains high. This result indicates that local environmental barriers to dispersal were decreasing in importance, rejecting previous suggestions that the rainforest collapse caused an “island biogeography” effect. Instead, dispersal at this time is restricted by continental-scale barriers, with the increased orogenic uplift as a possible control.

The origin of modern amphibians: a re-evaluation

There are currently three competing hypotheses seeking to explain the evolutionary origins of modern amphibians. The lepospondyl hypothesis holds that the lysorophian lepospondyls constitute the sister taxon to all lissamphibians. The temnospondyl hypothesis suggests that modern amphibians are most closely related to the dissorophoid temnospondyls. Finally, the polyphyletic hypothesis posits that the modern amphibian orders have separate evolutionary origins from among different groups of Palaeozoic tetrapods. Here, we review the character matrices used in previous studies. These data sets differ significantly in choice of characters. Therefore, we built a matrix based on data from all three hypotheses and analysed key taxa phylogenetically using both Bayesian inference and parsimony. Uncorrected, the supermatrix yielded inconclusive results, demonstrating the presence of at least two phylogenetic optima. When the data were corrected according to new observations on Doleserpeton, Eocaecilia, and other fossil forms, the phylogeny supported the temnospondyl hypothesis of lissamphibian origins. This conclusion is also supported by a careful study of character changes in the individual lineages.

Bystrow’s Paradox - gills, fossils, and the fish-to-tetrapod transition

Schoch, R.R. and Witzmann, F. 2011. Bystrow’s Paradox – gills, fossils, and the fish-to-tetrapod transition. —Acta Zoologica (Stockholm) 92: 251–265. The issue of which breathing mechanism was used by the earliest tetrapods is still unsolved. Recent discoveries of stem tetrapods suggest the presence of internal gills and fish-like underwater breathing. The same osteological features were used by Bystrow to infer a salamander-like breathing through external gills in temnospondyl amphibians. This apparent contradiction – here called Bystrow’s Paradox – is resolved by reviewing the primary fossil evidence and the anatomy of the two gill types in extant taxa. Rather unexpectedly, we find that internal gills were present in a range of early crown tetrapods (temnospondyls), based on the anatomy of gill lamellae and location of branchial arteries on the ventral side of gill arch elements (ceratobranchials). Although it remains to be clarified which components are homologous in external and internal gills, both gill types are likely to have been present in Palaeozoic tetrapods – internal gills in aquatic adults of some taxa, and external gills in the larvae of these taxa and in larvae of numerous forms with terrestrial adults, which resorbed the external gills after the larval phase. Future developmental studies will hopefully clarify which mechanistic pathways are involved in gill formation and how these might have evolved.

Osteology and relationships of the temnospondyl genusSclerocephalus

The temnospondyl Sclerocephalus from the Permo-Carboniferous of Germany is one of the most completely preserved and most abundant Palaeozoic tetrapods. Here, we review the complete osteology of the genus, based on a range of fully grown specimens housed in public collections. Among the four valid species, Sclerocephalus haeuseri and Sclerocephalus nobilis reached an adult size of well beyond 1 m in length, and had robust postcranial skeletons. In the skull, the exoccipital and sphenethmoid bones were ossified, completing the well-known ossification sequence in S. haeuseri. Large adults had an elongate trunk and a laterally compressed tail, and some individuals also retained lateral line sulci: features that taken together suggest an aquatic life. The coracoid, pubis, carpals, tarsals, and the bony tail are fully ossified in the largest specimens. The genus Sclerocephalus forms a weakly supported clade nesting firmly at the base of the Stereospondylomorpha, and the close resemblance between Sclerocephalus, Onchiodon, and Eryops is found to be partially based on shared derived states, but is mostly based on symplesiomorphies. Cladistic analysis of 54 characters and 18 taxa finds more support for the Eryopoidea hypothesis (Eryopidae + Stereospondylomorpha) than for the Euskelia hypothesis (Eryopidae + Zatracheidae + Dissorophoidea). This indicates that the large temnospondyls of the Permian and Mesozoic probably formed a natural group, and that the terrestrial adaptations of Eryops and the dissorophoids probably evolved by convergence.

Linked morphological changes during palate evolution in early tetrapods

We examined the shapes and sizes of dermal bones of the palate of selected Palaeozoic tetrapods in order to identify the ancestral states of palatal bone morphologies in the earliest tetrapods, to learn how the composition of the palate varies within and among early tetrapod radiations, and to recognize evolutionary correlations among the size and shapes of skeletal elements in this important group of animals. We find that whereas the palatal bones themselves and their arrangements are usually conserved, considerable correlated evolutionary change occurs in the shapes and sizes of the bones. Some of the changes in the bones are allometrically linked to overall palate size, which varies more than 100-fold among the taxa in our sample. Often, these allometries were only hinted at in traditional independent contrasts-based regressions of log transformed data, particularly because many allometries are subtle, their slopes may vary among subclades, and the scatter around some trendlines is high. Rather, the allometries showed up in analyses of size-standardized palatal bone dimensions investigated using independent contrasts, bivariate phylomorphospace plots, and mirrored character reconstructions on the phylogenetic tree. We find negative allometry for parasphenoid lengths and widths essentially across the entire tree of Palaeozoic tetrapods, but with different trajectories characterizing the two largest clades, the temnospondyls and the lepospondyls. The lengths of several other elements may show positive allometries, either across the entire tree or in just a subclade. One possible positive allometry exists for the ectopterygoid, which appears to shorten allometrically in temnospondyls that evolve small body and palate size, and, as in Doleserpeton can be lost altogether. Both shortening and loss could be by the same developmental change, paedomorphosis, a form of heterochrony. Paedomorphosis might also account for evolution of relatively large parasphenoids in both lepospondyls and diminutive temnospondyls, but does not seem to explain evolution of ectopterygoid loss in lepospondyls. A regularity observed across nearly all taxa in our study set is an inverse correlation between the lengths of the vomer and pterygoid, bones that lie adjacent to one another along the long palatal axis. Further work is needed to learn whether such correlated evolution might be due to adaptation and/or to developmental bias, and particularly to learn how correlations and allometries themselves evolve.

A supertree of early tetrapods

A genus-level supertree for early tetrapods is built using a matrix representation of 50 source trees. The analysis of all combined trees delivers a long-stemmed topology in which most taxonomic groups are assigned to the tetrapod stem. A second analysis, which excludes source trees superseded by more comprehensive studies, supports a deep phylogenetic split between lissamphibian and amniote total groups. Instances of spurious groups are rare in both analyses. The results of the pruned second analysis are mostly comparable with those of a recent, character-based and large-scale phylogeny of Palaeozoic tetrapods. Outstanding areas of disagreement include the branching sequence of lepospondyls and the content of the amniote crown group, in particular the placement of diadectomorphs as stem diapsids. Supertrees are unsurpassed in their ability to summarize relationship patterns from multiple independent topologies. Therefore, they might be used as a simple test of the degree of corroboration of nodes in the contributory analyses. However, we urge caution in using them as a replacement for character-based cladograms and for inferring macroevolutionary patterns.

The Permian mammal-like herbivore Diictodon, the oldest known example of sexually dimorphic armament.

Dicynodonts, a highly successful group of Palaeozoic tetrapods, were herbivores with keratinous beaks, and were frequently equipped with large, neomorphic tusks. Diictodon is a particularly abundant dicynodont genus, allowing statistical investigation of its palaeobiology. Anatomical, morphometric and distributional analyses provide evidence of sexual dimorphism, based on the presence or absence of formidable tusks. Tusk occurrence is also correlated with the presence of a cranial boss on the skull roof and, possibly, with greater cranial size. This earliest well-documented example of dimorphic armament suggests that sexual dimorphism, and the complex social behaviour that accompanies it, have long been characteristic of the synapsid lineage.

The tetrapod Caerorhachis bairdi Holmes and Carroll from the Lower Carboniferous of Scotland

ABSTRACTThe tetrapod Caerorhachis bairdi, probably from the Pendleian Limestone Coal Group in the Scottish Midland Valley, is rediagnosed and redescribed, and its affinities are discussed. Caerorachis was originally interpreted as a temnospondyl amphibian, based on characters that are now regarded as primitive for tetrapods, or of uncertain polarity. Several features of Caerorhachis (e.g. gastrocentrous vertebrae, curved trunk ribs, reduced dorsal iliac blade, L-shaped tarsal intermedium) are observed in certain primitive amniotes. In particular, Caerorhachis resembles ‘anthracosaurs’, generally considered to be among the most primitive of stem-group amniotes.The phylogenetic position of Caerorhachis is considered in the light of recently published cladistic analyses of Palaeozoic tetrapods. Most analyses place Caerorhachis at the base of, or within, ‘anthracosaurs’. When multiple, equally parsimonious solutions are found, its ‘anthracosaur’ affinities are shown in at least some trees, and are supported by several informative and, generally, highly consistent characters. Alternative phylogenetic placements (e.g. sister taxon to temnospondyls) are usually less well corroborated.If the fundamental evolutionary split of most early tetrapods into stem-group lissamphibians (e.g. temnospondyls) and stem-group amniotes (e.g. ‘anthracosaurs’) is accepted, then the revised interpretation of Caerprhachis sheds light on near-ancestral conditions for Amniota.

Morphology of the atlas-axis complex of the late Palaeozoic tetrapod suborders Diadectomorpha and Seymouriamorpha

The atlas-axis complexes of the better-known genera of the Permo-Pennsylvanian tetrapod suborder Diadectomorpha are described and compared with those of other late Palaeozoic tetrapods. One new synapomorphy of the Diadectomorpha is identified: a large, anteriorly directed, midventral, projection of the axial intercentrum that articulates with a midventral furrow on the posterior margin of the atlantalintercentrum . Within the Diadectomorpha diadectids are apomorphic in possessing a large, anteriorly tapering axial neural spine, that accounts for approximately 40% of the total height of the axis;Limnoscelisis apomorphic in having divided parapophyseal facets of the atlantal intercentrum and anteriorly directed ventral processes of the atlantal intercentrum . Relative to the atlas-axis complex in the more primitive amphibian suborder Seymouriamorpha, that of diadectomorphs and other basal amniotes share two derived features: the atlantal pleurocentrum is fused to the dorsal surface of the axial intercentrum , except inTseajaiawhere the elements are not fused but are positioned similarly; and the axial pleurocentrum and neural arch are fused in all observable stages of ontogeny. Reinterpretation of the atlantal neural arch inSeymouriaindicates that it does not possess neural spines, a feature it shares with the Diadectomorpha and basal amniotes.