Bone Histology Reveals a High Environmental and Metabolic Plasticity as a Successful Evolutionary Strategy in a Long-Lived Homeostatic Triassic Temnospondyl

Evolutionary stasis (long-term stability of morphology in an evolving lineage) is a pattern for which explanations are usually elusive. The Triassic tetrapod Gerrothorax pulcherrimus, a gill-bearing temnospondyl, survived for 35 million years in the Germanic Basin of Central Europe persisting throughout the dinosaur-dominated Late Triassic period. This evolutionary stasis coincides with the occurrence of this species in a wide range of habitats and environmental conditions. By the combination of palaeoecological and palaeohistological analyses, we found great ecological flexibility in G. pulcherrimus and present substantial evidence of developmental and metabolic plasticity despite the morphological stasis. We conclude that G. pulcherrimus could show the capacity to settle in water bodies too harsh or unpredictable for most other tetrapods. This would have been made possible by a unique life history strategy that involved a wide reaction norm, permitting adjustment to fluctuating conditions such as salinity and level of nutrients. Growth rate, duration of juvenile period, age at maturity, and life span were all subject to broad variation within specimens of G. pulcherrimus in one single lake and in between different lakes. In addition to providing a better understanding of fossil ecosystems, this study shows the potential of such a methodology to encourage palaeobiologists and evolutionary biologists to consider the mechanisms of variation in extant and fossil organisms by using a similar time-scope reference.     

Braincase,palatoquadrate and ear region of the plagiosaurid Gerrothorax pulcherrimus from the Middle Triassic of Germany

Abstract: The complete neurocranium plus palatoquadrate of the plagiosaurid temnospondyl Gerrothorax pulcherrimus from the Middle Triassic of Germany is described for the first time, based on outer morphological observations and micro‐CT scanning. The exoccipitals are strong elements with paroccipital processes and well‐separated occipital condyles. Anterolaterally, the exoccipitals contact the otics, which are mediolaterally elongated and have massive lateral walls. The otics contact the basisphenoid, which shows well‐developed sellar processes. Anteriorly, the basisphenoid is continuous with the sphenethmoid region. In its posterior portion, the sphenethmoid gives rise to robust, laterally directed laterosphenoid walls, a unique morphology among basal tetrapods. The palatoquadrate is extensively ossified. The quadrate portion overlaps the descending lamina of squamosal and ascending lamina of pterygoid anteriorly, almost contacting the epipterygoid laterally. The epipterygoid is a complex element and may be co‐ossified with otics and laterosphenoid walls. It has a broad, sheet‐like footplate and a horizontally aligned ascending process that contacts the laterosphenoid walls. The degree of ossification of the epipterygoid, however, is subject to individual variation obviously independent from ontogenetic changes. The stapes of Gerrothorax is a large, blade‐like element that differs conspicuously from the plesiomorphic temnospondyl condition. It has a prominent anterolateral projection which has not been observed in other basal tetrapods. Morphology of neurocranium and palatoquadratum of Gerrothorax most closely resembles that of the Russian plagiosaurid Plagiosternum danilovi, although the elements are less ossified in the latter. The extensive endocranial ossification of Gerrothorax is consistent with the general high degree of ossification in the exo‐ and endoskeleton of this temnospondyl and supports the view that a strong endocranial ossification cannot be evaluated as a plesiomorphic character in basal tetrapods.     

The plagiosaurid temnospondyl Plagiosuchus pustuliferus (Amphibia: Temnospondyli) from the Middle Triassic of Germany: anatomy and functional morphology of the skull

The cranial anatomy of the plagiosaurid temnospondyl Plagiosuchus pustuliferus, from the Middle Triassic of Germany, is described in detail on the basis of a newly discovered skull and mandibular material. The highly derived skull is characterized by huge orbitotemporal fenestrae, a reduction of the circumorbital bones – the prefrontal, postfrontal and (probably) postorbital are lost – and the expansion of the jugal to occupy most of the lateral skull margin. Ventrally the extremely long subtemporal vacuities correlate with the elongate adductor fossa of the mandible. The dentition is feebly developed on both skull and mandible. Ossified ?ceratobranchials and ‘branchial denticles’ indicate the presence of open gills clefts in life. The remarkably divergent cranial morphology of P. pustuliferus highlights the extraordinary cranial diversity within the Plagiosauridae, probably unsurpassed within the Temnospondyli. Specific structural aspects of the skull – including an extremely short marginal tooth row, feeble dentition and an elongated chamber for adductor musculature – together with evidence for a hyobranchial skeleton, suggests that P. pustuliferus utilized directed suction feeding for prey capture. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 348–373.     

Craniodental variation among Macaques (Macaca), nonhuman primates

Background  

In terms of structure and function, the skull is one of the most complicated organs in the body. It is also one of the most important parts in terms of developmental and evolutionary origins. This complexity makes it difficult to obtain evolutionary assessments if, as is usually the case with fossils, only part of the skull is available. For this reason this study involves a set of comparisons whereby the smallest functional units are studied first, and these built up, through a triple-nested hierarchical design, into more complex anatomical regions and eventually into the skull-as-a-whole. This design has been applied to macaques (Macaca) in order to reveal patterns of variation at the different levels. The profiles of such variation have been obtained both within and between species. This has lead to a search for the skull parts that have undergone similar selection pressures during evolution and comparable development patterns in both ontogeny and phylogeny.     

Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae,Caimaninae)

Melanosuchus niger is a caimanine alligatorid widely distributed in the northern region of South America. This species has been the focus of several ecological, genetic and morphological studies. However, morphological studies have generally been limited to examination of interspecific variation among extant species of South American crocodylians. Here, we present the first study of intraspecific variation in the skull of M. niger using a two‐dimensional geometric morphometric approach. The crania of 52 sexed individuals varying in size were analysed to quantify shape variation and to assign observed shape changes to different types of intraspecific variation, that is, ontogenetic variation and sexual dimorphism. Most of the variation in this species is ontogenetic variation in snout length, skull depth, orbit size and the width of the postorbital region. These changes are correlated with bite force performance and probably dietary changes. However, a comparison with previous functional studies reveals that functional adaptations during ontogeny seem to be primarily restricted to the postrostral region, whereas rostral shape changes are more related to dietary shifts. Furthermore, the skulls of M. niger exhibit a sexual dimorphism, which is primarily size‐related. The presence of non‐size‐related sexual dimorphism has to be tested in future examinations.     

Skull morphology and phylogenetic relationships of a new Middle Triassic plagiosaurid temnospondyl from Germany,and the evolution of plagiosaurid eyes

A partial skull from the Lower Keuper (Middle Triassic) of Germany is recognized as belonging to a new genus and species of plagiosaurid temnospondyl. It is readily identified by the following autapomorphies: (1) extremely large orbits medially extended to give very thin interorbital region and cheek; (2) posterior skull table abbreviated, with splint‐like supratemporals, postparietals and parietals; (3) supraorbital lateral line sulcus absent on frontal, with blind ending on parietal, and continued at the anterior margin of the postorbital; (4) occiput sloping posteriorly, with subtympanic fossa exposed in ventral view; (5) cultriform process and basicranial suture extremely narrow; (6) mandibular and maxillary teeth very long with crowns markedly curved inwards. The new taxon shares the following derived character states with Plagiosternum: (1) the pentagonal shape of orbits; (2) the slender interorbital region and cultriform process; (3) the small‐scale, polygonal pit‐and‐ridge ornament on posterior skull table, with single prominent tubercles rising from ridges. Phylogenetic analysis finds plagiosaurids to be monophyletic within a broad range of temnospondyls, nesting within a clade of short‐skulled stereospondyls. Plagio‐suchus is the most basal plagiosaurid, and Plagiosternum forms the sister group to the new taxon. The biological significance of the large orbits of plagiosaurids and their relationships to the eyeballs is discussed. The only type of eyeball that would be feasible for all known plagiosaurids would be a small spherical structure possibly situated near the anterior edge of the orbit. For those plagiosaurs with extremely large shallow orbits like Plagiosternum and Megalophthalma, a possible adaptation would be a lens‐less eye comprising a flat retinal plate across the entire orbit.     

Timing of ontogenetic changes of two cranial regions in Sotalia guianensis (Delphinidae)

Despite the fact that heterochronic processes seem to be an important process determining morphological evolution of the delphinid skull, previous workers have not found allometric scaling as relevant factor in the differentiation within the genus Sotalia. Here we analyzed the skull ontogeny of the estuarine dolphin S. guianensis and investigate differential growth and shape changes of two cranial regions – the neurocranium and the face – in order to evaluate the relevance of cranial compartmentalization on the ontogeny of this structure. Our results show that, even though both cranial regions stop growing at adulthood, the face has higher initial growth rates than the neurocranium. The rate of shape changes is also different for both regions, with the face showing a initially higher, but rapidly decreasing rate of change, while the neurocranium shows a slow decreasing rate, leading to persistent and localized shape changes throughout adult life, a pattern that could be related to epigenetic regional factors. The pattern of ontogenetic shape change described here is similar to those described for other groups of Delphinidae and also match intra and interspecific variation found within the family, suggesting that mosaic heterochrony could be an important factor in the morphological evolution of this group.     

Tooth and cranial disparity in the fossil relatives of Sphenodon (Rhynchocephalia) dispute the persistent ‘living fossil’ label

The tuatara (Sphenodon punctatus) is the only living representative of Rhynchocephalia, a group of small vertebrates that originated about 250 million years ago. The tuatara has been referred to as a living fossil; however, the group to which it belongs included a much greater diversity of forms in the Mesozoic. We explore the morphological diversity of Rhynchocephalia and stem lepidosaur relatives (Sphenodon plus 13 fossil relatives) by employing a combination of geometric morphometrics and comparative methods. Geometric morphometrics is used to explore cranium size and shape at interspecific scale, while comparative methods are employed to test association between skull shape and size and tooth number after taking phylogeny into account. Two phylogenetic topologies have been considered to generate a phylomorphospace and quantify the phylogenetic signal in skull shape data, the ancestral state reconstruction as well as morphological disparity using disparity through time plots (DTT). Rhynchocephalia exhibit a significant phylogenetic signal in skull shape that compares well with that computed for other extinct vertebrate groups. A consistent form of allometry has little impact on skull shape evolution while the number of teeth significantly correlates with skull shape also after taking phylogeny into account. The ancestral state reconstruction demonstrates a dramatic shape difference between the skull of Sphenodon and its much larger Cretaceous relative Priosphenodon. Additionally, DTT demonstrates that skull shape disparity is higher between rather than within clades while the opposite applies to skull size and number of teeth. These results were not altered by the use of competing phylogenic hypotheses. Rhynchocephalia evolved as a morphologically diverse group with a dramatic radiation in the Late Triassic and Early Jurassic about 200 million years ago. Differences in size are not marked between species whereas changes in number of teeth are associated with co‐ordinated shape changes in the skull to accommodate larger masticatory muscles. These results show that the tuatara is not the product of evolutionary stasis but that it represents the only survivor of a diverse Mesozoic radiation whose subsequent decline remains to be explained.     

Patterns of intraspecific variation through ontogeny: a case study of the Cretaceous nautilid Eutrephoceras dekayi and modern Nautilus pompilius

The magnitude and ontogenetic patterns of intraspecific variation can provide important insights into the evolution and development of organisms. Understanding the intraspecific variation of organisms is also a key to correctly pursuing studies in major fields of palaeontology. However, intraspecific variation has been largely overlooked in ectocochleate cephalopods, particularly nautilids. Furthermore, little is known regarding the evolutionary pattern. Here, we present morphological data for the Cretaceous nautilid Eutrephoceras dekayi (Morton) and the modern nautilid Nautilus pompilius Linnaeus through ontogeny. The data are used to describe conch morphology and to elucidate the evolutionary patterns of intraspecific variation. We discovered a similar overall pattern of growth trajectories and the presence of morphological changes at hatching and maturity in both taxa. We also found that intraspecific variation is higher in earlier ontogeny than in later ontogeny in both taxa. The high variation in earlier ontogeny may imply increased flexibility in changing the timing of developmental events, which probably played an important role in nautilid evolution. We assume that the decrease in variation in later ontogeny reflects developmental constraints. Lastly, we compared the similarity/dissimilarity of ontogenetic patterns of variation between taxa. Results reveal that the similarity/dissimilarity of the ontogenetic pattern differs between E. dekayi and N. pompilius. We conclude that this shift in the ontogenetic pattern of variation may be rooted in changes in the developmental programme of nautilids through time. We propose that studying ontogenetic patterns of intraspecific variation can provide new insights into the evolution and development of organisms.     

The Evolution of Modularity in the Mammalian Skull II: Evolutionary Consequences

Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.     

Morphometric study of allometric skull growth in the temnospondyl Archegosaurus decheni from the Permian/Carboniferous of Germany

The skulls of ninety-six specimens of the temnospondyl Archegosaurus decheni from the Permian/Carboniferous of Germany, ranging in length from almost 20 to almost 280 mm, are used in a morphometric analysis of cranial ontogeny. A Cartesian transformation, a bivariate regression analysis, and a principal component analysis (PCA) reveal changes of general skull proportions and of particular skull roofing bones during growth. The preorbital part of the skull exhibits a much faster growth rate than the postorbital region, whereas the orbits exhibit a considerable decrease in relative size. The skull bones possess low allometry coefficients of growth in width, what leads to a proportionally much more slender skull than in most other temnospondyls, comparable only to other archegosaurids, the cochleosaurid Chenoprosopus, and longirostrine stereospondyls like Australerpeton and trematosaurids. Distinctly negative allometry of the width of the cheek region, where part of the adductor musculature originated, suggests a weaker bite in A. decheni than in temnospondyls with broad-parabolic skulls like Onchiodon and Sclerocephalus. Results from the analysis of skull growth in A. decheni offer a biological interpretation of the life habits of this animal as becoming increasingly more adaptated to piscivory during ontogeny. The continuous growth of the skull with a gradual shift in proportions supports, in conjunction with morphological data, the hypothesis that A. decheni did not undergo a metamorphosis.     

Testing evolutionary stasis and trends in first lower molar shape of extinct Italian populations of Terricola savii (Arvicolidae,Rodentia) by means of geometric morphometrics

Extinct populations of Terricola savii have been investigated in order to analyse evolutionary stasis and correlation of first lower molar shape with climatic proxies by means of geometric morphometrics. Evolutionary stasis, its recognition and explanation are central topics in evolutionary paleobiology. In this study, tooth shape variation of the arvicolid T. savii has been analysed through time. In addition to explicit multivariate tests of stasis based on landmark and semi‐landmark geometric morphometrics, first lower molar M₁ shape has been decomposed in orthogonal axes of variation and tested for correlation with climate changes. Multivariate tests were consistent with evolutionary stasis. Yet, according to univariate tests, the dominant dimension of shape variation shows a temporal trend well correlated with a climatic proxy, i.e. δ¹⁸O. The remaining variation does not show any trend. Adaptation to current climatic condition might occur even without affecting shape as a whole. Phenotypic plasticity of this species could be invoked to explain evolutionary stasis, as a long time pattern.     

A farewell to arms and legs: a review of limb reduction in squamates

Elongated snake-like bodies associated with limb reduction have evolved multiple times throughout vertebrate history. Limb-reduced squamates (lizards and snakes) account for the vast majority of these morphological transformations, and thus have great potential for revealing macroevolutionary transitions and modes of body-shape transformation. Here we present a comprehensive review on limb reduction, in which we examine and discuss research on these dramatic morphological transitions. Historically, there have been several approaches to the study of squamate limb reduction: (i) definitions of general anatomical principles of snake-like body shapes, expressed as varying relationships between body parts and morphometric measurements; (ii) framing of limb reduction from an evolutionary perspective using morphological comparisons; (iii) defining developmental mechanisms involved in the ontogeny of limb-reduced forms, and their genetic basis; (iv) reconstructions of the evolutionary history of limb-reduced lineages using phylogenetic comparative methods; (v) studies of functional and biomechanical aspects of limb-reduced body shapes; and (vi) studies of ecological and biogeographical correlates of limb reduction. For each of these approaches, we highlight their importance in advancing our understanding, as well as their weaknesses and limitations. Lastly, we provide suggestions to stimulate further studies, in which we underscore the necessity of widening the scope of analyses, and of bringing together different perspectives in order to understand better these morphological transitions and their evolution. In particular, we emphasise the importance of investigating and comparing the internal morphology of limb-reduced lizards in contrast to external morphology, which will be the first step in gaining a deeper insight into body-shape variation.     

The impact of metamorphosis on the cranial osteology of giant salamanders of the genus Dicamptodon

Pacific giant salamanders (Dicamptodon) rank among the largest terrestrial caudates. Their ontogeny produces two distinct morphs—larval‐neotenic and metamorphosed—which differ in many morphological traits. We identified changes that are initiated by metamorphosis (distinguishing transformed from neotenic specimens) and also recognized age‐related changes occurring irrespective of transformation. During metamorphosis, specimens remodel the palate, rearrange the vomerine dentition, expand the maxilla, broaden the cheek, foreshorten the posterior skull table and develop specific serrated suture patterns in the dermal bones. Instead, large larvae grow a robust pterygoid sutured with a fully ossified trapezoidal vomer and a short maxilla. Small larvae are readily distinguished by tooth count, morphology and arrangement from more advanced larvae. Age‐related features, irrespective of metamorphosis, include pedicellate teeth, morphological differentiation of parasphenoid, enlargement of the orbitosphenoid, distal expansion of columella, and loss of coronoid teeth.     

Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation

Xiphosurids are an archaic group of aquatic chelicerate arthropods, generally known by the colloquial misnomer of ‘horseshoe crabs’. Known from marine environments as far back as the early Ordovician, horseshoe crabs are generally considered ‘living fossils’ – descendants of a bradytelic lineage exhibiting little morphological or ecological variation throughout geological time. However, xiphosurids are known from freshwater sediments in the Palaeozoic and Mesozoic; furthermore, the contention that xiphosurids show little morphological variation has never been tested empirically. Attempts to test this are hampered by the lack of a modern phylogenetic framework with which to explore different evolutionary scenarios. Here, I present a phylogenetic analysis of Xiphosurida and explore patterns of morphospace and environmental occupation of the group throughout the Phanerozoic. Xiphosurids are shown to have invaded non‐marine environments independently at least five times throughout their evolutionary history, twice resulting in the radiation of major clades – bellinurines and austrolimulids – that occupied novel regions of morphospace. These clades show a convergent ecological pattern of differentiation, speciation and subsequent extinction. Horseshoe crabs are shown to have a more dynamic and complex evolutionary history than previously supposed, with the extant species representing only a fraction of the group's past ecological and morphological diversity.     

Anterior sensory organs in Sabellariidae (Annelida)

Sensory organs in Annelida are very diverse and may be useful for assessments of morphological adaptation and character evolution. We used several methods to provide new insights into processes underlying the evolutionary radiation of anterior sensory organs in Sabellariidae. The presence and morphological diversity of the median organ (MO) found in the group was reviewed in order to test its phylogenetic significance and possible relationships to the distribution and ecological traits of the lineages. To test the intraspecific phenotypic plasticity of the MO, molecular analyses were conducted that focused on mitochondrial and nuclear genes from populations of Idanthyrsus australiensis exhibiting variation in the morphology of the MO. We used an integrative microscopical study of the ontogeny of Sabellaria alveolata to describe the anterior sensory structures present in the larvae and the morphological changes occurring before, during, and after settlement. In larval stages, the palps and the dorsal hump (DH) exhibit distinct innervation. The larval DH organ, which is likely to play a major role in chemoreception for settlement, is interpreted as being the incipient form of the adult MO. These results suggest that annelid sensory organs including the MO may be useful for phylogenetic and developmental investigations.     

Calvarial suture interdigitation in hadrosaurids (Ornithischia: Ornithopoda): Perspectives through ontogeny and evolution

Lambeosaurine hadrosaurids exhibited extreme modifications to the skull, where the premaxillae, nasals, and prefrontals were modified to form their iconic supracranial crests. This morphology contrasts with their sister group, Hadrosaurinae, which possessed the plesiomorphic arrangement of bones. Although studies have discussed differences between lambeosaurine and hadrosaurine skull morphology and ontogeny, there is little information detailing suture modifications through ontogeny and evolution. Suture morphology is of particular interest due to its correlation with the mechanical loading of the skull in extant vertebrates. We quantify and contrast the morphology of calvarial sutures in iguanodontians and ontogenetic series of Corythosaurus and Gryposaurus to test whether the evolution of lambeosaurine crests impacted the mechanical loading of the skull. We found that suture interdigitation (SI) increases through ontogeny in hadrosaurids, although this increase is more extreme in Corythosaurus than Gryposaurus, and overall suture complexity (i.e., overall shape) remained constant. Lambeosaurines also have higher SI than other iguanodontians, even in crestless juveniles, suggesting that increased sinuosity is unrelated to the structural support of the crest. Hadrosaurines and basal iguanodontians did not differ. Similarly, lambeosaurines have more complexly shaped sutures than hadrosaurines and basal iguanodontians, while the latter two groups do not differ. Taken together, these results suggest that lambeosaurine calvarial sutures are more interdigitated than other iguanodontians, and although suture sinuosity increased through ontogeny, the suture shape remained constant. These ontogenetic and evolutionary patterns suggest that increased suture complexity in lambeosaurines coincided with crest evolution, and corresponding modifications to their facial skeleton altered the distribution of stress while feeding.     

Differences in shape and size of skull and mandible in Talpa species (Mammalia: Eulipotyphla) from Turkey

We analysed with landmark-based images morphological differences between four species of Talpa which resemble each other morphologically and are all highly adapted to underground life. Subtle shape differences of the skull and mandibular bones were found between all species. However, there is also broad overlap between all species. Talpa caucasica had the largest skull and mandibles, and Talpa levantis the smallest.