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Early Amniotes and Their Close Relatives
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Amniotes include mammals, reptiles and birds, representing 75% of extant vertebrate species on land. They originated around 318 million years ago in the early Late Carboniferous and their early fossil record is central to understanding the expansion of vertebrates in terrestrial ecosystems. We present a phylogenetic hypothesis that challenges the widely accepted consensus about early amniote evolution, based on parsimony analysis and Bayesian inference of a new morphological dataset. We find a reduced membership of the mammalian stem lineage, which excludes varanopids. This implies that evolutionary turnover of the mammalian stem lineage during the Early–Middle Permian transition (273 million years ago) was more abrupt than has previously been recognized. We also find that Parareptilia are nested within Diapsida. This suggests that temporal fenestration, a key structural innovation with important functional implications, evolved fewer times than generally thought, but showed highly variable morphology among early reptiles after its initial origin. Our phylogeny also addresses controversies over the affinities of mesosaurids, the earliest known aquatic amniotes, which we recover as early diverging parareptiles. A new amniote phylogeny excludes varanopids as stem-line mammals, nests Parareptilia within Diapsida and suggests that temporal fenestration evolved fewer times than previously thought.
Histology and microanatomy of vertebrae, ribs, haemal
arch, and humeri and femora of 10 individuals of Stereosternum and two dorsal ribs of
1 individual of Brazilosaurus were studied. All individuals had achieved a body length
of 50 cm (equal to 65 % of the maximum known body length) or larger. All sampled
bones are highly osteosclerotic due to the reduction of medullary cavities
and the filling of medullary regions by endosteal bone. Calcified cartilage
occurs – if at all – only locally in small clusters in the medullary
regions of midshaft and in higher amounts only in non-midshaft sections of
long bones and towards the medio-distal rib shaft, respectively. The primary
bone tissue consists of highly organized parallel-fibred tissue and/or
lamellar tissue, which is in most samples relatively lightly vascularized or
even avascular. If present, vascular canals are mainly longitudinally
oriented; some show a radial orientation. Simple vascular canals as well as
primary osteons occur. Some of the latter are secondarily altered, i.e. widened. Remodelling of the periosteal cortex is only documented by few
scattered erosion cavities and secondary osteons. The tissue is regularly
stratified by lines of arrested growth (LAGs), which usually appear as double or multiple rest lines,
indicating strong dependence on exogenous and endogenous factors. Because of
the inhibition of periosteal remodelling the growth record is complete and
no inner cycles are lost. Individuals of Stereosternum show a poor correlation of body
size and number of growth marks, which might be the result of developmental
plasticity. Brazilosaurus shows a highly organized, avascular lamellar tissue and a high
number of regularly deposited rest lines throughout the cortex of the ribs.
The medullary region in the ribs of Brazilosaurus is distinctly larger when compared to ribs
of Stereosternum. However, strong osteosclerosis is obvious in both taxa, pointing to a
high degree of aquatic adaption. Ribs of Stereosternum, Brazilosaurus, and Mesosaurus are clearly distinguishable
from each other by the distribution of the periosteal and endosteal
territory. Furthermore, Brazilosaurus differs in its growth pattern (i.e. spacing of rest
lines) when compared to Stereosternum and Mesosaurus.
Pareiasaurs were one of the main clades of large herbivorous tetrapods in Middle–Late Permian continental ecosystems. Despite abundant pareiasaur material, many aspects of their biology remain poorly known. This paper provides a description of ontogenetic changes in long-bone and rib microanatomy/histology of two Upper Permian pareiasaurs from Russia, Deltavjatia rossica and Scutosaurus karpinskii. Analysis of a growth series of bones of Deltavjatia and Scutosaurus revealed rapid and cyclical growth early in ontogeny (as indicated by fast-growing fibrolamellar bone with lines of arrested growth). This was followed by a change in the growth pattern (as indicated by an outer avascular layer of lamellar bone in the cortex) and a decrease in the growth rate after 50% of maximum body size was reached in Deltavjatia and 75% in Scutosaurus (larger body sizes in Scutosaurus were attained through an extended initial period of fast skeletal growth). The study confirms that the bones of all pareiasaurs are histologically and microanatomically uniform [spongious (porous) microstructure and a very thin compact cortex] and indicate a similar growth strategy (a short initial period of rapid and cyclical growth followed by a long period of slow growth). The microanatomical characteristics of pareiasaurs do not provide a clear indication of their lifestyle.
Provelosaurus americanus from the Guadalupian of Brazil, is the only species of pareiasaur known from South America and its studies are limited to anatomical descriptions. Here, we examined the microstructure of limb bones, a rib fragment and osteoderms of P. americanus, aiming to answer questions related to its paleobiology. The bone tissues of this specimen comprise poorly vascularised parallel-fibred bone interrupted by growth marks indicating slow, cyclical growth. This is consistent with the pattern found in other pareisaurs from South Africa. However, the space between the LAGs are irregular and there is no clear decreasing in vascularity toward the periphery of the bone, suggesting that it did not reach skeletal maturity. The highest number of LAGs was found in the rib, suggesting that our sample lived a minimum of fifteen years. The osteoderms present a trilaminar structure consisting of a diploe composed of a cancellous core surrounded by two cortical layers. A diploe is absent from the osteoderms of previously studied South African pareiasaurs. The osteogenesis of the osteoderms is intramembraneous, but a metaplastic ossification during the early developmental stage cannot be entirely discarded, due to extensive remodeling in the central core that could have destroyed potential metaplastic tissue.
The early Permian cave system in the Dolese Brothers Limestone Quarry near Richards Spur, Oklahoma represents a unique depositional environment that has been interpreted as preserving an upland biota. The quarry and the region around it represent Paleozoic cave systems that underwent periods of flooding not unlike present-day conditions that are commonly associated with monsoonal episodes. The Richards Spur locality is particularly rich in captorhinid eureptiles which represent one of the earliest reptilian clades to have evolved a specialized dentition. Although the multiple-tooth rowed Captorhinus aguti is the most abundant captorhinid at Richards Spur, at least one other species has been described (Captorhinus magnus) and assigned to the same genus, but five other captorhinid taxa have also been found. We describe a new member of the genus Captorhinus (Captorhinus kierani) and explore details of the dental anatomy against the two other members of the genus at Richards Spur, C. aguti and C. magnus, as well as with a member of the genus not presently known from Richards Spur (Captorhinus laticeps). Findings suggest that the nature of the ogival dentition described previously as a synapomorphy uniting C. aguti with C. magnus is not supported and we propose a more informative method for differentiating among dental characters within the clade. The discovery of a new species of Captorhinus provides additional evidence for captorhinid taxic diversity at Richards Spur and is supportive of niche partitioning, which is likely associated with reducing intra-specific competition within the clade. In addition, we argue that the captorhinid fossils at Richards Spur likely includes one additional, currently undescribed multiple-tooth rowed form, that renders the current practice of assigning disarticulated cranial remains, specifically dental fragments, to the species C. aguti problematic. Finally, we offer a method for a comprehensive examination of the dental characteristics, which can then be applied to explore taxic diversity at Richards Spur and examine one of the earliest examples of niche specialization. As a consequence of this research, additional insight into exploring biological interactions between Paleozoic taxa can be examined, with an opportunity to shed light on what might have driven these evolutionary processes.
The largest published phylogenetic analysis of early limbed vertebrates (Ruta M, Coates MI. 2007. Journal of Systematic Palaeontology 5:69–122) recovered, for example, Seymouriamorpha, Diadectomorpha and (in some trees) Caudata as paraphyletic and found the “temnospondyl hypothesis” on the origin of Lissamphibia (TH) to be more parsimonious than the “lepospondyl hypothesis” (LH)—though only, as we show, by one step. We report 4,200 misscored cells, over half of them due to typographic and similar accidental errors. Further, some characters were duplicated; some had only one described state; for one, most taxa were scored after presumed relatives. Even potentially continuous characters were unordered, the effects of ontogeny were not sufficiently taken into account, and data published after 2001 were mostly excluded. After these issues are improved—we document and justify all changes to the matrix—but no characters are added, we find (Analysis R1) much longer trees with, for example, monophyletic Caudata, Diadectomorpha and (in some trees) Seymouriamorpha; Ichthyostega either crownward or rootward of Acanthostega; and Anthracosauria either crownward or rootward of Temnospondyli. The LH is nine steps shorter than the TH (R2; constrained) and 12 steps shorter than the “polyphyly hypothesis” (PH—R3; constrained). Brachydectes (Lysorophia) is not found next to Lissamphibia; instead, a large clade that includes the adelogyrinids, urocordylid “nectrideans” and aïstopods occupies that position. As expected from the taxon/character ratio, most bootstrap values are low. Adding 56 terminal taxa to the original 102 increases the resolution (and decreases most bootstrap values). The added taxa range in completeness from complete articulated skeletons to an incomplete lower jaw. Even though the lissamphibian-like temnospondyls Gerobatrachus, Micropholis and Tungussogyrinus and the extremely peramorphic salamander Chelotriton are added, the difference between LH (R4; unconstrained) and TH (R5) rises to 10 steps, that between LH and PH (R6) to 15; the TH also requires several more regains of lost bones than the LH. Casineria, in which we tentatively identify a postbranchial lamina, emerges rather far from amniote origins in a gephyrostegid-chroniosuchian grade. Bayesian inference (Analysis EB, settings as in R4) mostly agrees with R4. High posterior probabilities are found for Lissamphibia (1.00) and the LH (0.92); however, many branches remain weakly supported, and most are short, as expected from the small character sample. We discuss phylogeny, approaches to coding, methods of phylogenetics (Bayesian inference vs. equally weighted vs. reweighted parsimony), some character complexes (e.g. preaxial/postaxial polarity in limb development), and prospects for further improvement of this matrix. Even in its revised state, the matrix cannot provide a robust assessment of the phylogeny of early limbed vertebrates. Sufficient improvement will be laborious—but not difficult.
Teeth and dentitions contain many morphological characters which give them a
particularly important weight in comparative anatomy, systematics, physiology and
ecology. As teeth are organs that contain the hardest mineralized tissues vertebrates
can produce, their fossil remains are abundant and the study of their anatomy in fossil
specimens is of major importance in evolutionary biology. Comparative anatomy has
long favored studies of dental characters rather than features associated with tooth
attachment and implantation. Here we review a large part of the historical and modern
work on the attachment, implantation and replacement of teeth in Amniota. We propose
synthetic definitions or redefinitions of most commonly used terms, some of which have
led to confusion and conflation of terminology. In particular, there has long been much
conflation between dental implantation that strictly concerns the geometrical aspects
of the tooth-bone interface, and the nature of the dental attachment, which mostly
concerns the histological features occurring at this interface. A second aim of this
work was to evaluate the diversity of tooth attachment, implantation and replacement in
extant and extinct amniotes in order to derive hypothetical evolutionary trends in these
different dental traits over time. Continuous dental replacement prevails within amniotes,
replacement being drastically modified only in Mammalia and when dental implantation
is acrodont. By comparison, dental implantation frequently and rapidly changes at
various taxonomic scales and is often homoplastic. This contrasts with the conservatism
in the identity of the tooth attachment tissues (cementum, periodontal ligament, and
alveolar bone), which were already present in the earliest known amniotes. Because the
study of dental attachment requires invasive histological investigations, this trait is least
documented and therefore its evolutionary history is currently poorly understood. Finally,
it is essential to go on collecting data from all groups of amniotes in order to better
understand and consequently better define dental characters.
The early amniote clade Mesosauridae has long been of interest to scientists, primarily due to the members of the clade being the oldest secondarily aquatic tetrapods and their role as a line of evidence for continental drift. In the landmark phylogenetic analysis of Parareptilia by Gauthier and colleagues in 1988, Mesosauridae was found to be the sister taxon of all included parareptiles. Over the last three decades several studies regarding the phylogenetic placement of mesosaurs have helped to reinforce their position as the most basal parareptile clade. The most recent study of Mesosauridae is by Laurin and Piñeiro, who reassess the phylogenetic position of the clade within early amniotes. This new analysis recovered mesosaurs as being the sister clade to all other sauropsids, supporting the results of an earlier study by Laurin and Reisz in 1995. However, we feel that there are two main issues with this new study that need to be addressed. The first is the use of an outdated phylogenetic matrix and the fact that the authors patently ignore over two decades of parareptilian research when conducting their phylogenetic analysis, whereas the second involves the problems associated with lateral temporal fenestration and its extreme variability in reptiles. We discuss how these two issues could have influenced the results that were obtained from this study, and how, when they are taken into account, a different picture regarding the phylogenetic position of Mesosauridae is reconstructed to that of Laurin and Piñeiro.
Mesosaurs have been considered strictly aquatic animals. Their adaptations to the aquatic environment are well known and include putative viviparity, along with the presence of several skeletal characters such as a long, laterally compressed tail, long limbs, the foot larger than the manus, and presence of pachyosteosclerotic bones. They were also described as possessing non-coossified girdle bones and incompletely ossified epiphyses, although there could be an early fusion of the front girdle bones to form the scapulocoracoid in some specimens. Some of these features, however, are shared by most basal tetrapods that are considered semiaquatic and even some terrestrial ones. The study of vertebral columns and limbs provides essential clues about the locomotor system and the lifestyle of early amniotes. In this study, we have found that the variation of the vertebral centrum length along the axial skeleton of Mesosaurus tenuidens fits better with a semi-aquatic morphometric pattern, as shown by comparisons with other extinct and extant taxa. The present study allows us to suggest that whereas well-preserved mesosaur skeletons are mostly represented by juveniles and young adults that inhabited aquatic environments, more mature individuals might hypothetically have spent time on land. This is also supported, to an extent, by taphonomic factors such as the scarce representation and poor preservation of remains of mature individuals in the fossiliferous levels, and also by anatomy of the appendicular bones, and particularly the strongly ossified epiphyses and tarsus.
Bone microstructure has long been known as a powerful tool to investigate lifestyle-related biomechanical constraints, and many studies have focused on identifying such constraints in the limb bones of aquatic or arboreal mammals in recent years. The limb bone microstructure of fossorial mammals, however, has not been extensively described. Furthermore, so far, studies on this subject have always focused on the bone histology of small burrowers, such as subterranean rodents or true moles. Physiological constraints associated with digging, however, are known to be strongly influenced by body size, and larger burrowers are likely to exhibit a histological profile more conspicuously influenced by fossorial activity. Here, we describe for the first time the limb bone histology of the aardvark (Orycteropus afer), the largest extant burrowing mammal. The general pattern is very similar for all six sampled limb bones (i.e., humerus, radius, ulna, femur, tibia, and fibula). Most of the cortex at midshaft is comprised of compacted coarse cancellous bone (CCCB), an endosteal tissue formed in the metaphyses through the compaction of bony trabeculae. Conversely, the periosteal bone is highly resorbed in all sections, and is reduced to a thin outer layer, suggesting a pattern of strong cortical drift. This pattern contrasts with that of most large mammals, in which cortical bone is of mostly periosteal origin, and CCCB, being a very compliant bone tissue type, is usually resorbed or remodeled during ontogeny. The link between histology and muscle attachment sites, as well as the influence of the semi-arid environment and ant-eating habits of the aardvark on its bone microstructure, are discussed. We hypothesize that the unusual histological profile of the aardvark is likely the outcome of physiological constraints due to both extensive digging behavior and strong metabolic restrictions. Adaptations to fossoriality are thus the result of a physiological compromise between limited food availability, an environment with high temperature variability, and the need for biomechanical resistance during digging. These results highlight the difficulties of deciphering all factors potentially involved in bone formation in fossorial mammals. Even though the formation and maintaining of CCCB through ontogeny in the aardvark cannot be unambiguously linked with its fossorial habits, a high amount of CCCB has been observed in the limb bones of other large burrowing mammals. The inclusion of such large burrowers in future histological studies is thus likely to improve our understanding of the functional link between bone growth and fossorial lifestyle in an evolutionary context.
Ontogenetic series of extinct taxa are rare. However, if preserved, fossil embryos and juveniles can provide evidence of developmental plasticity as related to ecological specialization. Here, we describe articulated and isolated juvenile material found in close association with an adult mesosaurid Stereosternum tumidum (MB.R.2089) from Lower Permian sediments in Brazil, housed in the collection of the Museum für Naturkunde Berlin. Stylopodial, zeugopodial, and autopodial elements are not yet completely ossified in the juveniles, as indicated by compression artifacts on the surface of the bone. These correspond to internal ossification processes, which have been demonstrated in other aquatic taxa. Quantitative analysis of measurements in juvenile and adult material reveals differing growth rates between limb elements: hind limb zeugopodia, which are massive and elongate in the adult as needed for propulsion, are already comparatively larger in the juvenile than the humeri, femora, and also the zeugopodia of the forelimb. This pattern differs from that seen in another extinct aquatic reptile, Hovasaurus boulei. Nevertheless, we attribute the accelerated growth rate or earlier onset of ossification to be a potential developmental pathway generating limb element variation in the adult present in 280 million year old mesosaurs, which are known for their fully aquatic lifestyle, in which the hind limbs play a more prominent role than the forelimbs.
We reassess the phylogenetic position of mesosaurs by using a data matrix that is updated and slightly expanded from a matrix that the first author published in 1995 with his former thesis advisor. The revised matrix, which incorporates anatomical information published in the last 20 years and observations on several mesosaur specimens (mostly from Uruguay) includes 17 terminal taxa and 129 characters (four more taxa and five more characters than the original matrix from 1995). The new matrix also differs by incorporating more ordered characters (all morphoclines were ordered). Parsimony analyses in PAUP 4 using the branch and bound algorithm show that the new matrix supports a position of mesosaurs at the very base of Sauropsida, as suggested by the first author in 1995. The exclusion of mesosaurs from a less inclusive clade of sauropsids is supported by a Bremer (Decay) index of 4 and a bootstrap frequency of 66%, both of which suggest that this result is moderately robust. The most parsimonious trees include some unexpected results, such as placing the anapsid reptile Paleothyris near the base of diapsids, and all of parareptiles as the sister-group of younginiforms (the most crownward diapsids included in the analyses). Turtles are placed among parareptiles, as the sister-group of pareiasaurs (and in diapsids, given that parareptiles are nested within diapsids). This unexpected result offers a potential solution to the long-lasting controversy about the position of turtles because previous studies viewed a position among diapsids and among parareptiles as mutually exclusive alternatives.
The evolution of herbivory in early tetrapods was crucial in the establishment of terrestrial ecosystems, although it is so far unclear what effect this innovation had on the macro-evolutionary patterns observed within this clade. The clades that entered this under-filled region of ecospace might be expected to have experienced an “adaptive radiation”: an increase in rates of morphological evolution and speciation driven by the evolution of a key innovation. However such inferences are often circumstantial, being based on the coincidence of a rate shift with the origin of an evolutionary novelty. The conclusion of an adaptive radiation may be made more robust by examining the pattern of the evolutionary shift; if the evolutionary innovation coincides not only with a shift in rates of morphological evolution, but specifically in the morphological characteristics relevant to the ecological shift of interest, then one may more plausibly infer a causal relationship between the two.
Here I examine the impact of diet evolution on rates of morphological change in one of the earliest tetrapod clades to evolve high-fibre herbivory: Captorhinidae. Using a method of calculating heterogeneity in rates of discrete character change across a phylogeny, it is shown that a significant increase in rates of evolution coincides with the transition to herbivory in captorhinids. The herbivorous captorhinids also exhibit greater morphological disparity than their faunivorous relatives, indicating more rapid exploration of new regions of morphospace. As well as an increase in rates of evolution, there is a shift in the regions of the skeleton undergoing the most change; the character changes in the herbivorous lineages are concentrated in the mandible and dentition. The fact that the increase in rates of evolution coincides with increased change in characters relating to food acquisition provides stronger evidence for a causal relationship between the herbivorous diet and the radiation event.
Patterns of bone development in mammals are best known from terrestrial and cursorial groups, but there is a considerable gap in our understanding of how specializations for life underground affect bone growth and development. Likewise, studies of bone microstructure in wild populations are still scarce, and they often include few individuals and tend to be focused on adults. For these reasons, the processes generating bone microstructural variation at intra- and interspecific levels are not fully understood. This study comprehensively examines the bone microstructure of an extant population of Cape dune molerats, Bathyergus suillus (Bathyergidae), the largest subterranean mammal endemic to the Western Cape of South Africa. The aim of this study is to investigate the postnatal bone growth of B. suillus using undecalcified histological sections (n = 197) of the femur, humerus, tibia-fibula, ulna and radius, including males and females belonging to different ontogenetic and reproductive stages (n = 42). Qualitative histological features demonstrate a wide histodiversity with thickening of the cortex mainly resulting from endosteal and periosteal bone depositions, whilst there is scarce endosteal resorption and remodeling throughout ontogeny. This imbalanced bone modeling allows the tissues deposited during ontogeny to remain relatively intact, thus preserving an excellent record of growth. The distribution of the different bone tissues observed in the cortex depends on ontogenetic status, anatomical features (e.g. muscle attachment structures) and location on the bone (e.g. anterior or lateral). The type of bone microstructure and modeling is discussed in relation to digging behavior, reproduction and physiology of this species. This study is the first histological assessment describing the process of cortical thickening in long bones of a fossorial mammal.
Studies of the effects of mass extinctions on ancient ecosystems have focused on changes in taxic diversity, morphological disparity, abundance, behaviour and resource availability as key determinants of group survival. Crucially, the contribution of life history traits to survival during terrestrial mass extinctions has not been investigated, despite the critical role of such traits for population viability. We use bone microstructure and body size data to investigate the palaeoecological implications of changes in life history strategies in the therapsid forerunners of mammals before and after the Permo-Triassic Mass Extinction (PTME), the most catastrophic crisis in Phanerozoic history. Our results are consistent with truncated development, shortened life expectancies, elevated mortality rates and higher extinction risks amongst post-extinction species. Various simulations of ecological dynamics indicate that an earlier onset of reproduction leading to shortened generation times could explain the persistence of therapsids in the unpredictable, resource-limited Early Triassic environments, and help explain observed body size distributions of some disaster taxa (e.g., Lystrosaurus). Our study accounts for differential survival in mammal ancestors after the PTME and provides a methodological framework for quantifying survival strategies in other vertebrates during major biotic crises.
Body size is an extremely important characteristic, impacting on a variety of ecological and life-history traits. It is therefore important to understand the factors which may affect its evolution, and diet has attracted much interest in this context. A recent study which examined the evolution of the earliest terrestrial herbivores in the Late Carboniferous and Early Permian concluded that in the four herbivorous clades examined there was a trend towards increased body size, and that this increase was more substantial than that observed in closely related carnivorous clades. However, this hypothesis was not based on quantitative examination, and phylogenetic comparative methods provide a more robust means of testing such hypotheses. Here, the evolution of body size within different dietary regimes is examined in Captorhinidae, the most diverse and longest lived of these earliest high fibre herbivores. Evolutionary models were fit to their phylogeny to test for variation in rate and mode of evolution between the carnivorous and herbivorous members of this clade, and an analysis of rate variation throughout the tree was carried out. Estimates of ancestral body sizes were calculated in order to compare the rates and direction of evolution of lineages with different dietary regimes. Support for the idea that the high fibre herbivores within captorhinids are being drawn to a higher adaptive peak in body size than the carnivorous members of this clade is weak. A shift in rates of body size evolution is identified, but this does not coincide with the evolution of high-fibre herbivory, instead occurring earlier in time and at a more basal node. Herbivorous lineages which show an increase in size are not found to evolve at a faster rate than those which show a decrease; in fact, it is those which experience a size decrease which evolve at higher rates. It is possible the shift in rates of evolution is related to the improved food processing ability of the more derived captorhinids rather than a shift in diet, but the evidence for this is circumstantial.
ABSTRACT—Pareiasaurs were a group of herbivorous reptiles that lived during the middle to late Permian (~265–252 Ma) in what is modern-day Europe, Asia, South America, and Africa. Field work in the Moradi Formation of northern Niger has produced multiple elements of the appendicular skeleton of the pareiasaur Bunostegos akokanensis. The considerable size disparity and morphological variation among the elements suggest that they represent ontogenetic stages ranging from relatively juvenile to adult. Here we present the first description of the scapulocoracoid, humerus, radius, ulna, pelvis, and femur of Bunostegos as well as some of the first ontogenetic data for postcranial osteology in pareiasaurs. As with the skull, numerous postcranial autapomorphies characterize Bunostegos, including laterally originating acromion process of the scapula; radius and ulna with continuous articular surface on humerus; paired crests on the olecranon process; ulna longer than humerus; pinched posterior margin of the acetabular rim; robust pelvic symphysis extending the length of the puboischiatic plate; lack of a distinct postaxial flange of the femur; and an elaborated femoral lateral condyle wrapping over the medial condyle. We incorporated data from the appendicular skeleton of Bunostegos into a revised phylogenetic analysis of pareiasaur relationships. The results of this analysis corroborate previous cranial analyses that place Bunostegos between Guadalupian taxa and the Lopingian velosaur subclade. Interestingly, several aspects of its postcranial anatomy suggest that Bunostegos possessed relatively upright forelimb posture, which would be unique among pareiasaurs and possibly Permian
amniotes as a whole.
Transitional fossils informing the origin of turtles are among the most sought-after discoveries in palaeontology. Despite strong genomic evidence indicating that turtles evolved from within the diapsid radiation (which includes all other living reptiles), evidence of the inferred transformation between an ancestral turtle with an open, diapsid skull to the closed, anapsid condition of modern turtles remains elusive. Here we use high-resolution computed tomography and a novel character/taxon matrix to study the skull of Eunotosaurus africanus, a 260-million-year-old fossil reptile from the Karoo Basin of South Africa, whose distinctive postcranial skeleton shares many unique features with the shelled body plan of turtles. Scepticism regarding the status of Eunotosaurus as the earliest stem turtle arises from the possibility that these shell-related features are the products of evolutionary convergence. Our phylogenetic analyses indicate strong cranial support for Eunotosaurus as a critical transitional form in turtle evolution, thus fortifying a 40-million-year extension to the turtle stem and moving the ecological context of its origin back onto land. Furthermore, we find unexpected evidence that Eunotosaurus is a diapsid reptile in the process of becoming secondarily anapsid. This is important because categorizing the skull based on the number of openings in the complex of dermal bone covering the adductor chamber has long held sway in amniote systematics, and still represents a common organizational scheme for teaching the evolutionary history of the group. These discoveries allow us to articulate a detailed and testable hypothesis of fenestral closure along the turtle stem. Our results suggest that Eunotosaurus represents a crucially important link in a chain that will eventually lead to consilience in reptile systematics, paving the way for synthetic studies of amniote evolution and development.
Captorhinids are inherently interesting Paleozoic reptiles because they include the first terrestrial vertebrates to have multiple tooth rows on the maxilla and dentary. This may have been a key innovation that allowed captorhinids to diversify and disperse throughout the Permian Period of Pangea. We provide the first comparison of tooth development in captorhinids to determine how multiple rows of marginal teeth evolved within this clade. By comparing thin sections of multiple-rowed Captorhinus aguti from the Lower Permian of Oklahoma with the contemporaneous, single-rowed Captorhinus magnus, we provide evidence for variation in jaw growth, which establishes the number of tooth rows. Comparisons with the basal captorhinid Concordia cunninghami from the Upper Carboniferous of Kansas demonstrate that early captorhinids retained the typical amniote condition of replacing teeth in a manner similar to modern iguanian lizards. By comparing tooth development in C. aguti with other single-rowed captorhinids, we also demonstrate that the shedding of old teeth and the development of new teeth are not linked developmental processes in captorhinids. Instead, the fates of older generations of teeth are entirely dependent on their proximity to the lingual surface of the dentary where the tooth-producing organ, the dental lamina, would have been present. These peculiar features of the dentitions of captorhinids make them model taxa for examining patterns of tooth development and replacement.
Pareiasaurs were globally distributed, abundant, herbivorous parareptiles of the Middle to Late Permian, with the basal-most members found in the Middle Permian of South Africa. These basal taxa were particularly abundant and went extinct at the end of the Gaudalupian (Capitanian) at the top of the Tapinocephalus Assemblage Zone. Currently four taxa are recognized in this group: Bradysaurus seeleyi, B. baini, Nochelesaurus alexanderi and Embrithosaurus schwarzi, but they are all poorly understood. We here present the first detailed cranial description and updated diagnosis for Embrithosaurus schwarzi. No cranial autapomorphies were identified. However, Embrithosaurus schwarzi is a distinct taxon in this group, based on its unique dentition and using a combination of cranial features. It has nine marginal cusps on all maxillary and mandibular teeth, and wider maxillary teeth than in the co-occurring taxa, due to the marginal cusps being arranged more regularly around the crown, and the apex of the crown lacking the long, central, three-cusped trident. Our updated phylogenetic analysis recovers the four Middle Permian South African taxa as a monophyletic group for the first time, which we call Bradysauria, comprising a clade including Embrithosaurus, Bradysaurus baini and a polytomy including Nochelesaurus and Bradysaurus seeleyi.
The Abrahamskraal Formation of South Africa has a diverse middle Permian (Guadalupian) fossil tetrapod fauna comprising largely basal therapsids and pareiasaurian parareptiles. Knowledge on the paleoecology of these animals is limited because inferences of many ecological traits in mid-Permian tetrapods are based on deductions from morphology. While it is widely accepted that the rhinesuchid amphibians were aquatic, the ecological lifestyle of pareiasaurs and dinocephalian therapsids remains uncertain. To investigate the ecological roles of different middle Permian tetrapod taxa we studied stable oxygen isotope compositions of phosphate from teeth and bones as a proxy for water dependence. Our results reveal similar δ¹⁸Op values for pareiasaurs, the dinocephalian Anteosaurus, and therocephalians, with a range of values similar to those of extant terrestrial species. The consistent δ¹⁸Op values for pareiasaurs strengthen our interpretation of a terrestrial lifestyle for these parareptiles, but the lower Anteosaurus δ¹⁸Op values might question the interpretation and a larger sample size may result in a more conclusive outcome. These results conclude the debate on the ecology of middle Permian pareiasaurs. A terrestrial lifestyle is applicable only to the middle Permian species and a different lifestyle is possible for pareiasaurs species that lived after the end Capitanian extinction.
Recent field work in the upper Permian Moradi Formation of Niger has yielded new material of the late-occurring and largest moradisaurine captorhinid, Moradisaurus grandis. The material includes two right hemimandibles, which represent individuals that are slightly smaller than the holotype. The smaller size of these mandibles, together with evidence in the form of tooth replacement, strongly suggest that the new material is ontogenetically younger than the holotype. The available evidence implies that tooth rows were added during growth in M. grandis. The mandible of M. grandis is distinguished from other moradisaurines in the extreme lingual extension of the tooth plate, which forms a dental shelf or plateau that supports the three lingual-most rows of teeth. In addition, a mentomeckelian bone is preserved, the first to be reported in a Paleozoic reptile. In contrast to the conspicuous wear documented on the teeth of certain other moradisaurines, wear facets are not observed on the teeth of the M. grandis specimens described here. The absence of tooth wear is surprising because the articular morphology of M. grandis is virtually identical to, albeit slightly larger than, that of Labidosaurikos meachami, for which propalinal jaw movement was first inferred in a moradisaurine. A phylogenetic analysis incorporating the new anatomical information confirms the hypothesis that M. grandis forms a clade with Rothianiscus multidontus and Gansurhinus qingtoushanensis within Moradisaurinae, and positions Captorhinikos chozaensis as the basal-most member of the subfamily.
Lystrosaurus is iconic for surviving the Permo-Triassic Mass Extinction and becoming the most abundant terrestrial vertebrate during the Early Triassic. Previous reports of skeletal remains of the Triassic species being found in fossilized burrows hint at a possible reason for its success, but unequivocal evidence showing that Lystrosaurus individuals were the burrow makers was lacking. I present here the first articulated skeleton of Lystrosaurus in a fossilized burrow from the Lower Triassic of the South African Karoo Basin, along with taphonomic evidence indicating that this individual was the burrow maker. The species is identified as L. curvatus, the only Lystrosaurus species recovered from above and below the inferred Permo-Triassic extinction horizon. It provides the first evidence of burrowing in a Permian species of Lystrosaurus, suggesting that this behavior was more prevalent than previously thought. Based on its size, the specimen is inferred to be a juvenile, showing that Lystrosaurus was capable of excavating burrows at young ontogenetic stages. The abundance of Lystrosaurus body fossils and similar-sized burrows from Lower Triassic strata suggests that burrowing played a pivotal role in the success of this genus in harsh, unpredictable postextinction conditions. Given the abundance of these burrows throughout the Lower Triassic Lystrosaurus Assemblage Zone, Lystrosaurus may have acted as an ecosystem engineer and refuge provider for other species, which may help to explain the high species diversity in the lowermost Triassic in the Karoo Basin.
SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP
Citation for this article: J. Botha-Brink. 2017. Burrowing in Lystrosaurus: preadaptation to a postextinction environment?. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2017.1365080.
We describe hindlimb elements of the large captorhinid Moradisaurus grandis (Reptilia: Captorhinidae) recently collected from the Upper Permian Moradi Formation of north-central Niger. This description is based primarily on an associated partial skeleton comprising a hemimandible, vertebral column, and partial left and nearly complete right hindlimb. Additionally, we report on a well-preserved, articulated, and essentially complete juvenile pes that provides important information on the ontogeny of the captorhinid tarsus. The hindlimb of Moradisaurus is stout and more massively built than in any other known captorhinid. The femur displays several features interpreted as adaptations to the demands of large body size, and the tibia and fibula have short, wide shafts and hypertrophied condyles and epicondyles. The astragalus is very derived, possessing two accessory ossifications and a relatively horizontal tibial articulation, indicating that the tibia was held more vertically than in other captorhinids. The calcaneum is co-ossified with distal tarsal five. The juvenile pes indicates that the captorhinid centrale arose from the fusion of two ossification centers, and that the captorhinid astragalus arose from the fusion of at least three ossification centers.
Numerous morphological studies have been carried out on pareiasaurs; yet their taxonomy and biology remain incompletely understood. Earlier works have suggested that these herbivorous parareptiles had a short juvenile period as compared to the duration of adulthood. Several studies further suggested an (semi-) aquatic lifestyle for these animals, but more recent investigations have proposed a rather terrestrial habitat. Bone paleohistology is regarded as a powerful tool to assess aspects of tetrapod paleobiology, but few studies have been conducted on pareiasaurs. The present study assesses intra and inter-specific histovariability of pareiasaurs and provides fresh insights into their paleobiology, thereby permitting a re-evaluation of earlier hypotheses. Our sample comprises various skeletal elements and several specimens covering most of the taxonomic and stratigraphic spectrum of South African pareiasaurs, including large and basal forms from the Middle Permian, as well as smaller and more derived forms from the Late Permian. Our results concerning size of elements and histological tissues show that for pareiasaurs, element size is not a good indicator of ontogenetic age, and furthermore, suggest that the specific diversity of the Middle Permian pareiasaurs may have been underestimated. The bone histology of these animals shows that they experienced a relatively rapid growth early in ontogeny. The periosteal growth later slowed down, but seems to have been protracted for several years during adulthood. Pareiasaur bone microanatomy is unusual for continental tetrapods, in having spongious stylopod diaphyses and thin compact cortices. Rigorous paleoecological interpretations are thus limited since no modern analogue exists for these animals. This article is protected by copyright. All rights reserved.
Numerous amniote groups adapted to an aquatic life. This change of habitat naturally led to numerous convergences. The various adaptive traits vary depending on the degree of adaptation to an aquatic life, notably between shallow water taxa still able to occasionally locomote on land and open-marine forms totally independent from the terrestrial environment, but also between surface swimmers and deep divers. As a consequence, despite convergences, there is a high diversity within aquatic amniotes in e.g., shape, size, physiology, swimming mode. Bone microanatomy is considered to be strongly associated with bone biomechanics and is thus a powerful tool to understand bone adaptation to functional constraints and to make functional inferences on extinct taxa. Two opposing major microanatomical specializations have been described in aquatic amniotes, referred to as bone mass increase and a spongious organization, respectively. They are assumed to be essentially linked with the hydrostatic or hydrodynamic control of buoyancy and body trim and with swimming abilities and velocity. However, between extremes in these specializations, a wide range of intermediary patterns occurs. The present study provides a state-of-the-art review of these inner bone adaptations in semi-aquatic and aquatic amniotes. The analysis of the various microanatomical patterns observed in long bones, vertebrae, and ribs of a large sample of (semi-)aquatic extant and extinct amniotes reveals the wide diversity in microanatomical patterns and the variation in combination of these different patterns within a single skeleton. This enables us to discuss the link between microanatomical features and habitat, swimming abilities, and thus functional requirements in the context of amniote adaptation to an aquatic lifestyle.
Although pareiasaurs are one of the most abundant and conspicuous elements of Late Permian terrestrial ecosystems, small individuals of these reptiles (either small species or juveniles of large species) are extremely rare. Until now, the smallest known pareiasaur is the type of the late, heavily armored form Anthodon (= Nanoparia ) pricei (Bernard Price Institute of Palaeontological Research, Johannesburg 1/6), with a skull length of 10 cm and an inferred snout-vent length of approximately 50 cm. This is presumably an adult of a dwarf form, since all elements of the skull and postcranial skeleton are fully ossified, sutures are closed, and the dermal armor is more highly developed than in any other pareiasaur (Broom and Robinson, 1948; Brink, 1955; Findlay, 1970; Lee, 1997). A second and as yet undescribed specimen (Geological Survey, Pretoria CM86/544) is approximately the same size, being only very slightly larger (Lee, 1997). No other specimens of this taxon are known. An unnumbered humerus in the Amalitsky collection of the Palaeontological Institute, Moscow, is from a pareiasaur of similar size to the second specimen of A. pricei. However, this specimen is presumably a juvenile of a large form: the ends of the humerus are unossified, and the specimen comes from the North Dvina bone beds, which have yielded numerous specimens of the large pareiasaur Scutosaurus but no other pareiasaur taxon. Here, we re-evaluate a specimen originally described as a dicynodont tail, and later as a procolophonoid, and demonstrate that it is actually a juvenile of the pareiasaur Elginia mirabilis. It is also by far the smallest pareiasaur so far known, being approximately half the dimensions of the next smallest individual, the type specimen of Anthodon pricei. The newly recognized specimen provides new information on the ontogeny of pareiasaurs and the homology of some problematic skull elements.
We have now positively identified a number of specimens of the formerly exclusively South American Stereosternum tumidum in the Great Karoo Basin of South Africa, and an osteological study has shown Mesosaurus tenuidens and M. braziliensis to be conspecific. The occurrence of the same mesosaurid species in the Southern African and South American Gondwana is of importance for 2 reasons: it constitutes the earliest record of a shared reptile species on different Gondwana continents, and it is the first record of a reptile species shared by Southern Africa and South America. Even the widespread genus Lystrosaurus, known from South Africa, Antarctica, India and China, has not yet been discovered in South America in spite of the recent discovery of other, only slightly older African genera such as Pareiasaurus and Procolophon in Brazil.-from Authors
This book had its origin when, about five years ago, an ecologist (MacArthur) and a taxonomist and zoogeographer (Wilson) began a dialogue about common interests in biogeography. The ideas and the language of the two specialties seemed initially so different as to cast doubt on the usefulness of the endeavor. But we had faith in the ultimate unity of population biology, and this book is the result. Now we both call ourselves biogeographers and are unable to see any real distinction between biogeography and ecology.
The species-level taxonomy of pareiasaurs is completely revised. The 49 described species are reduced to 17: Bradysaurus baini, Bradysaurus seeleyi, Nochelesaurus alexanderi, Embrithosaurus schwarzi, Deltavjatia vjatkensis, Shansisaurus xuecunensis, Shihtienfenia permica, Pareiasuchus peringueyi, Pareiasuchus nasicornis, Pareiasaurus serridens, Scutosaurus karpinskii, Sanchuansaurus pygmaeus, Elginia mirabilis, Provelosaurus americanus, Nanoparia luckhoffi, Anthodon serrarius, and Pumiliopareia pricei. All the other existing taxa are either junior synonyms of the above taxa, or based on indeterminate material, or based on non-pareiasaur material. Two new species are identified. The "rhipaeosaurids", previously considered to be primitive pareiasaurs, are a heterogenous assemblage of therapsids, nycteroleterids, and seymouriamorphs. In pareiasaurs, postcranial features prove to be at least as diagnostic as cranial features, but have been largely ignored by all previous workers. Previous estimates of species diversity in pareiasaurs and other Permian tetrapods have been grossly overinflated, erroneously implying the existence of unusual community structure. This taxonomic revision also reveals that pareiasaurs suffered two major extinctions during the Upper Permian. The first occurred at the end of the Tapinocephalus zone. Pareiasaurs then radiated from a single surviving lineage, before their final extinction at the Permo-Triassic boundary.
Parareptilien stellen ein artenreiches Monophylum paläozoischer und früh-mesozoischer Amnioten dar; sie bilden innerhalb der Reptilien die Schwestergruppe zu den Eureptilien. Pareiasaurier, eine Untergruppe der Parareptilien, sind eine bedeutende Komponente spät-permischer …kosysteme. Jüngst wurde ein Schwestergruppenverhältnis zu den Nycyeroletern entdeckt, mit welchen sie die "Pareiasauromorpha" bilden. Diese Arbeit befasst sich mit der Beschreibung einiger dieser bisher schlecht untersuchten Parareptilien und deren Verwandtschaftsverhältnisse.Der Pareiasaurier Deltavjatia vjatkensis und der Nycteroleter Emeroleter levis aus der russischen Lokalität Kotel''nich werden mithilfe neu entdeckten Materials im Detail beschrieben. Das gut erhaltene Deltavjatja Materials umfasst mehrere Grössenstadien und erlaubt eine Analyse der Wachstumsraten. Eine geometrisch-morphometrische Analyse des Schädeldachs lässt eine allometrische Zunahme von Schnauzenlänge und Postorbitalregion erkennen. Auch wird der historisch erste Pareiasaurier, Parasaurus geinitzi, aus dem oberpermischen Kupferschiefer von Deutschland neu beschrieben. Zudem ergibt eine Neuanalyse der russischen Nycteroleter eine Synonymie von Tokosaurus perforatus und Macroleter poezicus. Eine phylogenetische Analyse unter Verwendung von Parsimonie und bayesischen Methoden ergibt eine basale Stellung von Parasaurus und eine Monophylie der Nycteroleter; letztere wird aber nur durch die Parsimonie unterstützt. Alle phylogenetischen Methoden ergeben jedoch eine Monophylie der Pareiasauromorpha. Eine strato-kladistische Analyse zeigt zudem eine ähnliche Topologie. Eine biogeographische Analyse der Pareiasauromorpha ergibt mehrfache Verbreitungsereignisse nach Russland und China. Diese stimmen überein mit denen anderer oberpermischer Gruppen, jedoch werden nur wenige dieser Ereignisse komplett bei allen Taxa gefunden.
The small-bodied stereospondyl Lydekkerina huxleyi, dominated the amphibian fauna of the South African Lower Triassic. Even though the anatomy of this amphibian has been well described, its growth strategies and lifestyle habits have remained controversial. Previous studies attributed the relative uniformity in skull sizes to a predominance of subadult and adult specimens recovered in the fossil record. Anatomical and taphonomic data suggested that the relatively small body-size of this genus, compared to its Permo-Triassic relatives, could be linked to a shortened, rapid developmental period as an adaptation to maintain successful breeding populations under harsh environmental conditions. Moreover, Lydekkerina's habitat has been hypothesized to be either aquatic or mainly terrestrial. The current study utilizes bone microstructure to re-assess previous hypotheses pertaining to the biology and ecology of Lydekkerina. Various skeletal elements of different-sized specimens are analyzed to understand its growth dynamics, intra-skeletal variability and lifestyle adaptations. Bone histology revealed that our sample comprises individuals at different ontogenetic stages i.e., juveniles to mature individuals. Our results show that these amphibians, despite exhibiting plasticity in growth, experienced an overall faster growth during early ontogeny (thereby attaining sexual maturity sooner), as compared to most other temnospondyls. The microanatomy of the long bones with their thick bone walls and distinctive medullary cavity suggests that Lydekkerina may have been amphibious with a tendency to be more terrestrial. Our study concludes that Lydekkerina employed a peculiar growth strategy and lifestyle adaptations, which enabled it to endure the harsh, dry conditions of the Early Triassic. This article is protected by copyright. All rights reserved.
© 2015 Wiley Periodicals, Inc.
The Karoo basin of South Africa exposes a succession of Upper Permian to Lower Triassic terrestrial strata containing abundant terrestrial vertebrate fossils. Paleomagnetic/magnetostratigraphic and carbon-isotope data allow sections to be correlated across the basin. With this stratigraphy, the vertebrate fossil data show a gradual extinction in the Upper Permian punctuated by an enhanced extinction pulse at the Permian-Triassic boundary interval, particularly among the dicynodont therapsids, coinciding with negative carbon-isotope anomalies.