Modern Vertebrates Research Articles

Resilience of the replacing dentition in adult reptiles

The dentition is critical to animal survival and teeth are present in modern vertebrates including teleost fish, sharks, amphibians, mammals and reptiles. The developmental processes that give rise to teeth are not just preserved through evolution but also share high level of similarity with the embryogenesis of other ectodermal organs. In this review we go beyond the embryonic phase of tooth development to life-long tooth replacement. We will address the origins of successional teeth, the location of putative tissue-resident stem cells, how de novo tooth formation continues throughout life and how teeth are shed in a spatially and temporally controlled manner. We review the evidence that the dental epithelium, which is the earliest recognizable dental structure in the reptilian dentition, serves as a putative niche for tissue-resident epithelial stem cells and recent molecular findings from transcriptomics carried out in reptilian dentitions. We discuss how odontoclasts resorb the primary tooth allowing eruption of the successional tooth. The reptiles, particularly lizards, are emerging as some of the most accessible animals to study tooth replacement which has relevance to evolution of the dentition and human dental disorders.

A vertebrate-wide catalogue of T1R receptors reveals diversity in taste perception

Taste is a vital chemical sense for feeding behaviour. In mammals, the umami and sweet taste receptors comprise three members of the taste receptor type 1 (T1R/TAS1R) family: T1R1, T1R2 and T1R3. Because their functional homologues exist in teleosts, only three TAS1R genes generated by gene duplication are believed to have been inherited from the common ancestor of bony vertebrates. Here, we report five previously uncharacterized TAS1R members in vertebrates, TAS1R4, TAS1R5, TAS1R6, TAS1R7 and TAS1R8, based on genome-wide survey of diverse taxa. We show that mammalian and teleost fish TAS1R2 and TAS1R3 genes are paralogues. Our phylogenetic analysis suggests that the bony vertebrate ancestor had nine TAS1Rs resulting from multiple gene duplications. Some TAS1Rs were lost independently in descendent lineages resulting in retention of only three TAS1Rs in mammals and teleosts. Combining functional assays and expression analysis of non-teleost fishes we show that the novel T1Rs form heterodimers in taste-receptor cells and recognize a broad range of ligands such as essential amino acids, including branched-chain amino acids, which have not been previously considered as T1R ligands. This study reveals diversity of taste sensations in both modern vertebrates and their ancestors, which might have enabled vertebrates to adapt to diverse habitats on Earth.

Interpreting the Evolutionary Echoes of a Protein Complex Essential for Inner-Ear Mechanosensation.

The sensory epithelium of the inner ear, found in all extant lineages of vertebrates, has been subjected to over 500 million years of evolution, resulting in the complex inner ear of modern vertebrates. Inner-ear adaptations are as diverse as the species in which they are found, and such unique anatomical variations have been well studied. However, the evolutionary details of the molecular machinery that is required for hearing are less well known. Two molecules that are essential for hearing in vertebrates are cadherin-23 and protocadherin-15, proteins whose interaction with one another acts as the focal point of force transmission when converting sound waves into electrical signals that the brain can interpret. This "tip-link" interaction exists in every lineage of vertebrates, but little is known about the structure or mechanical properties of these proteins in most non-mammalian lineages. Here, we use various techniques to characterize the evolution of this protein interaction. Results show how evolutionary sequence changes in this complex affect its biophysical properties both in simulations and experiments, with variations in interaction strength and dynamics among extant vertebrate lineages. Evolutionary simulations also characterize how the biophysical properties of the complex in turn constrain its evolution and provide a possible explanation for the increase in deafness-causing mutants observed in cadherin-23 relative to protocadherin-15. Together, these results suggest a general picture of tip-link evolution in which selection acted to modify the tip-link interface, although subsequent neutral evolution combined with varying degrees of purifying selection drove additional diversification in modern tetrapods.

Vertebrate cranial evolution: Contributions and conflict from the fossil record.

In modern vertebrates, the craniofacial skeleton is complex, comprising cartilage and bone of the neurocranium, dermatocranium and splanchnocranium (and their derivatives), housing a range of sensory structures such as eyes, nasal and vestibulo-acoustic capsules, with the splanchnocranium including branchial arches, used in respiration and feeding. It is well understood that the skeleton derives from neural crest and mesoderm, while the sensory elements derive from ectodermal thickenings known as placodes. Recent research demonstrates that neural crest and placodes have an evolutionary history outside of vertebrates, while the vertebrate fossil record allows the sequence of the evolution of these various features to be understood. Stem-group vertebrates such as Metaspriggina walcotti (Burgess Shale, Middle Cambrian) possess eyes, paired nasal capsules and well-developed branchial arches, the latter derived from cranial neural crest in extant vertebrates, indicating that placodes and neural crest evolved over 500 million years ago. Since that time the vertebrate craniofacial skeleton has evolved, including different types of bone, of potential neural crest or mesodermal origin. One problematic part of the craniofacial skeleton concerns the evolution of the nasal organs, with evidence for both paired and unpaired nasal sacs being the primitive state for vertebrates.

Thyroid and endostyle development in cyclostomes provides new insights into the evolutionary history of vertebrates

BackgroundThe endostyle is an epithelial exocrine gland found in non-vertebrate chordates (amphioxi and tunicates) and the larvae of modern lampreys. It is generally considered to be an evolutionary precursor of the thyroid gland of vertebrates. Transformation of the endostyle into the thyroid gland during the metamorphosis of lampreys is thus deemed to be a recapitulation of a past event in vertebrate evolution. In 1906, Stockard reported that the thyroid gland in hagfish, the sister cyclostome group of lampreys, develops through an endostyle-like primordium, strongly supporting the plesiomorphy of the lamprey endostyle. However, the findings in hagfish thyroid development were solely based on this single study, and these have not been confirmed by modern molecular, genetic, and morphological data pertaining to hagfish thyroid development over the last century.ResultsHere, we showed that the thyroid gland of hagfish undergoes direct development from the ventrorostral pharyngeal endoderm, where the previously described endostyle-like primordium was not found. The developmental pattern of the hagfish thyroid, including histological features and regulatory gene expression profiles, closely resembles that found in modern jawed vertebrates (gnathostomes). Meanwhile, as opposed to gnathostomes but similar to non-vertebrate chordates, lamprey and hagfish share a broad expression domain of Nkx2-1/2-4, a key regulatory gene, in the pharyngeal epithelium during early developmental stages.ConclusionsBased on the direct development of the thyroid gland both in hagfish and gnathostomes, and the shared expression profile of thyroid-related transcription factors in the cyclostomes, we challenge the plesiomorphic status of the lamprey endostyle and propose an alternative hypothesis where the lamprey endostyle could be obtained secondarily in crown lampreys.

Comparative Approaches in Vertebrate Cartilage Histogenesis and Regulation: Insights from Lampreys and Hagfishes

Jawed vertebrates (gnathostomes) have been the dominant lineage of deuterostomes for nearly three hundred fifty million years. Only a few lineages of jawless vertebrates remain in comparison. Composed of lampreys and hagfishes (cyclostomes), these jawless survivors are important systems for understanding the evolution of vertebrates. One focus of cyclostome research has been head skeleton development, as its evolution has been a driver of vertebrate morphological diversification. Recent work has identified hyaline-like cartilage in the oral cirri of the invertebrate chordate amphioxus, making cyclostomes critical for understanding the stepwise acquisition of vertebrate chondroid tissues. Our knowledge of cyclostome skeletogenesis, however, has lagged behind gnathostomes due to the difficulty of manipulating lamprey and hagfish embryos. In this review, we discuss and compare the regulation and histogenesis of cyclostome and gnathostome skeletal tissues. We also survey differences in skeletal morphology that we see amongst cyclostomes, as few elements can be confidently homologized between them. A recurring theme is the heterogeneity of skeletal morphology amongst living vertebrates, despite conserved genetic regulation. Based on these comparisons, we suggest a model through which these mesenchymal connective tissues acquired distinct histologies and that histological flexibility in cartilage existed in the last common ancestor of modern vertebrates.

Foretelling the Flex-Vertebral Shape Predicts Behavior and Ecology of Fishes.

One key evolutionary innovation that separates vertebrates from invertebrates is the notochord, a central element that provides the stiffness needed for powerful movements. Later, the notochord was further stiffened by the vertebrae, cartilaginous, and bony elements, surrounding the notochord. The ancestral notochord is retained in modern vertebrates as intervertebral material, but we know little about its mechanical interactions with surrounding vertebrae. In this study, the internal shape of the vertebrae-where this material is found-was quantified in 16 species of fishes with various body shapes, swimming modes, and habitats. We used micro-computed tomography to measure the internal shape. We then created and mechanically tested physical models of intervertebral joints. We also mechanically tested actual vertebrae of five species. Material testing shows that internal morphology of the centrum significantly affects bending and torsional stiffness. Finally, we performed swimming trials to gather kinematic data. Combining these data, we created a model that uses internal vertebral morphology to make predictions about swimming kinematics and mechanics. We used linear discriminant analysis (LDA) to assess the relationship between vertebral shape and our categorical traits. The analysis revealed that internal vertebral morphology is sufficient to predict habitat, body shape, and swimming mode in our fishes. This model can also be used to make predictions about swimming in fishes not easily studied in the laboratory, such as deep sea and extinct species, allowing the development of hypotheses about their natural behavior.

Ecomorphological diversification of squamates in the Cretaceous.

Squamates (lizards and snakes) are highly successful modern vertebrates, with over 10 000 species. Squamates have a long history, dating back to at least 240 million years ago (Ma), and showing increasing species richness in the Late Cretaceous (84 Ma) and Early Palaeogene (66–55 Ma). We confirm that the major expansion of dietary functional morphology happened before these diversifications, in the mid-Cretaceous, 110–90 Ma. Until that time, squamates had relatively uniform tooth types, which then diversified substantially and ecomorphospace expanded to modern levels. This coincides with the Cretaceous Terrestrial Revolution, when angiosperms began to take over terrestrial ecosystems, providing new roles for plant-eating and pollinating insects, which were, in turn, new sources of food for herbivorous and insectivorous squamates. There was also an early Late Cretaceous (95–90 Ma) rise in jaw size disparity, driven by the diversification of marine squamates, particularly early mosasaurs. These events established modern levels of squamate feeding ecomorphology before the major steps in species diversification, confirming decoupling of diversity and disparity. In fact, squamate feeding ecomorphospace had been partially explored in the Late Jurassic and Early Cretaceous, and jaw innovation in Late Cretaceous squamates involved expansions at the extremes of morphospace.

The evolutionary origins of the vertebrate olfactory system.

Vertebrates develop an olfactory system that detects odorants and pheromones through their interaction with specialized cell surface receptors on olfactory sensory neurons. During development, the olfactory system forms from the olfactory placodes, specialized areas of the anterior ectoderm that share cellular and molecular properties with placodes involved in the development of other cranial senses. The early-diverging chordate lineages amphioxus, tunicates, lampreys and hagfishes give insight into how this system evolved. Here, we review olfactory system development and cell types in these lineages alongside chemosensory receptor gene evolution, integrating these data into a description of how the vertebrate olfactory system evolved. Some olfactory system cell types predate the vertebrates, as do some of the mechanisms specifying placodes, and it is likely these two were already connected in the common ancestor of vertebrates and tunicates. In stem vertebrates, this evolved into an organ system integrating additional tissues and morphogenetic processes defining distinct olfactory and adenohypophyseal components, followed by splitting of the ancestral placode to produce the characteristic paired olfactory organs of most modern vertebrates.

Do paleontologists dream of electric dinosaurs? Investigating the presumed inefficiency of dinosaurs contact incubating partially buried eggs

AbstractTroodon formosus, a theropod from the Late Cretaceous, is one of the few species of dinosaurs with multiple nest sites uncovered. It has been consistently demonstrated that eggs within these nests would have been partially buried in life—an exceedingly rare state in modern vertebrates. There has been debate over Troodon's capacity to engage in thermoregulatory contact incubation, especially regarding an adult's ability to efficiently supply partially buried eggs with energy. An actualistic investigation was undertaken to determine the thermodynamic efficiency of contact incubating partially buried eggs. An efficient system would keep eggs at temperatures closer to the surrogate parent than the ambient, without prohibitively high energy input. For the experiment, a surrogate dinosaur was created and used in both indoor controlled ambient temperature trials and in an outdoor variant. Even with ambient temperatures that were likely cooler than Cretaceous averages, the results showed that contact incubating partially buried eggs did seem to confer an energetic advantage; egg temperatures remained closer to the surrogate than ambient in both indoor and outdoor tests. Still, critics of contact incubating partially buried eggs are correct in that there is a depth at which adult energy would fail to make much of an impact—perhaps more relevant to buried eggs, as partially buried eggs would be in contact with an adult and likely above the thermal input threshold. Additionally, results from this experiment provide evidence for a possible evolutionary path from guarding behavior to thermoregulatory contact incubation.

Synchrotron x‐ray fluorescence analysis reveals diagenetic alteration of fossil melanosome trace metal chemistry

AbstractA key feature of the pigment melanin is its high binding affinity for trace metal ions. In modern vertebrates trace metals associated with melanosomes, melanin‐rich organelles, can show tissue‐specific and taxon‐specific distribution patterns. Such signals preserve in fossil melanosomes, informing on the anatomy and phylogenetic affinities of fossil vertebrates. Fossil and modern melanosomes, however, often differ in trace metal chemistry; in particular, melanosomes from fossil vertebrate eyes are depleted in Zn and enriched in Cu relative to their extant counterparts. Whether these chemical differences are biological or taphonomic in origin is unknown, limiting our ability to use melanosome trace metal chemistry to test palaeobiological hypotheses. Here, we use maturation experiments on eye melanosomes from extant vertebrates and synchrotron rapid scan‐x‐ray fluorescence analysis to show that thermal maturation can dramatically alter melanosome trace element chemistry. In particular, maturation of melanosomes in Cu‐rich solutions results in significant depletion of Zn, probably due to low pH and competition effects with Cu. These results confirm fossil melanosome chemistry is susceptible to alteration due to variations in local chemical conditions during diagenesis. Maturation experiments can provide essential data on melanosome chemical taphonomy required for accurate interpretations of preserved chemical signatures in fossils.

Diversified regulation of circadian clock gene expression following whole genome duplication.

Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called 'clock genes', collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.

Evolution of vertebrate gill covers via shifts in an ancient Pou3f3 enhancer

Whereas the gill chambers of jawless vertebrates open directly into the environment, jawed vertebrates evolved skeletal appendages that drive oxygenated water unidirectionally over the gills. A major anatomical difference between the two jawed vertebrate lineages is the presence of a single large gill cover in bony fishes versus separate covers for each gill chamber in cartilaginous fishes. Here, we find that these divergent patterns correlate with the pharyngeal arch expression of Pou3f3 orthologs. We identify a deeply conserved Pou3f3 arch enhancer present in humans through sharks but undetectable in jawless fish. Minor differences between the bony and cartilaginous fish enhancers account for their restricted versus pan-arch expression patterns. In zebrafish, mutation of Pou3f3 or the conserved enhancer disrupts gill cover formation, whereas ectopic pan-arch Pou3f3b expression generates ectopic skeletal elements resembling the multimeric covers of cartilaginous fishes. Emergence of this Pou3f3 arch enhancer >430 Mya and subsequent modifications may thus have contributed to the acquisition and diversification of gill covers and respiratory strategies during gnathostome evolution.

Novel developmental bases for the evolution of hypobranchial muscles in vertebrates

BackgroundVertebrates are characterized by possession of hypobranchial muscles (HBMs). Cyclostomes, or modern jawless vertebrates, possess a rudimentary and superficial HBM lateral to the pharynx, whereas the HBM in jawed vertebrates is internalized and anteroposteriorly specified. Precursor cells of the HBM, marked by expression of Lbx1, originate from somites and undergo extensive migration before becoming innervated by the hypoglossal nerve. How the complex form of HBM arose in evolution is relevant to the establishment of the vertebrate body plan, but despite having long been assumed to be similar to that of limb muscles, modification of developmental mechanisms of HBM remains enigmatic.ResultsHere we characterize the expression of Lbx genes in lamprey and hagfish (cyclostomes) and catshark (gnathostome; jawed vertebrates). We show that the expression patterns of the single cyclostome Lbx homologue, Lbx-A, do not resemble the somitic expression of mammalian Lbx1. Disruption of Lbx-A revealed that LjLbx-A is required for the formation of both HBM and body wall muscles, likely due to the insufficient extension of precursor cells rather than to hindered muscle differentiation. Both homologues of Lbx in the catshark were expressed in the somitic muscle primordia, unlike in amniotes. During catshark embryogenesis, Lbx2 is expressed in the caudal HBM as well as in the abdominal rectus muscle, similar to lamprey Lbx-A, whereas Lbx1 marks the rostral HBM and pectoral fin muscle.ConclusionsWe conclude that the vertebrate HBM primarily emerged as a specialized somatic muscle to cover the pharynx, and the anterior internalized HBM of the gnathostomes is likely a novelty added rostral to the cyclostome-like HBM, for which duplication and functionalization of Lbx genes would have been a prerequisite.

Lampreys, “Living Fossils,” in Research on Early Development and Regeneration in Vertebrates

Agnathans, the most ancient of the extant vertebrates, evoke steadily increasing interest as the object of research on the basic processes of vertebrate ontogeny. Lampreys have been more accessible to researchers than myxines (hagfish), representatives of the other class of jawless vertebrates, for more than 100 years. Studies on the functional and evolutionary aspects of early ontogeny in lamprey at the molecular level became possible in the past two decades. Studies on the distinctive features of lampreys as the ancient representatives of vertebrates and comparison to gnathostomes, the more modern vertebrates, are of great interest. Molecular studies of lampreys can provide insight into the evolutionary mechanisms for the emergence and development of individual unique structures of vertebrates. The appearance of the telencephalon, which was first detected in lampreys, was one of the most important aromorphoses of vertebrates. Development and advancement of the telencephalon in the course of evolution enabled the implementation of higher forms of nervous activity in vertebrates, including humans. Research on the molecular mechanisms of basic ontogenetic events, such as early embryonic differentiation and neural induction, in the lamprey and other vertebrates is also important. Studies on the well-developed regeneration capacity of lampreys, in turn, give hope for at least partial use of the knowledge gained in future medical practice. This article is a review of recent data on the molecular aspects of the early development of the telencephalon, early embryonic differentiation, and regeneration of lampreys.

Archosauromorph extinction selectivity during the Triassic–Jurassic mass extinction

AbstractMany traits have been linked to extinction risk among modern vertebrates, including mode of life and body size. However, previous work has indicated there is little evidence that body size, or any other trait, was selective during past mass extinctions. Here, we investigate the impact of the Triassic–Jurassic mass extinction on early Archosauromorpha (basal dinosaurs, crocodylomorphs and their relatives) by focusing on body size and other life history traits. We built several new archosauromorph maximum‐likelihood supertrees, incorporating uncertainty in phylogenetic relationships. These supertrees were then employed as a framework to test whether extinction had a phylogenetic signal during the Triassic–Jurassic mass extinction, and whether species with certain traits were more or less likely to go extinct. We find evidence for phylogenetic signal in extinction, in that taxa were more likely to become extinct if a close relative also did. However, there is no correlation between extinction and body size, or any other tested trait. These conclusions add to previous findings that body size, and other traits, were not subject to selection during mass extinctions in closely‐related clades, although the phylogenetic signal in extinction indicates that selection may have acted on traits not investigated here.

Digitizing extant bat diversity: An open-access repository of 3D μCT-scanned skulls for research and education.

Biological specimens are primary records of organismal ecology and history. As such, museum collections are invaluable repositories for testing ecological and evolutionary hypotheses across the tree of life. Digitizing and broadly sharing the phenotypic data from these collections serves to expand the traditional reach of museums, enabling widespread data sharing, collaboration, and education at an unprecedented scale. In recent years, μCT-scanning has been adopted as one way for efficiently digitizing museum specimens. Here, we describe a large repository of 3D, μCT-scanned images and surfaces of skulls from 359 extant species of bats, a highly diverse clade of modern vertebrates. This digital repository spans much of the taxonomic, biogeographic, and morphological diversity present across bats. All data have been published to the MorphoSource platform, an online database explicitly designed for the archiving of 3D morphological data. We demonstrate one potential use of this repository by testing for convergence in skull shape among one particularly diverse group of bats, the superfamily Noctilionoidea. Beyond its intrinsic utility to bat biologists, our digital specimens represent a resource for educators and for any researchers seeking to broadly test theories of trait evolution, functional ecology, and community assembly.

A tetrapod fauna from within the Devonian Antarctic Circle.

Until now, all known fossils of tetrapods (limbed vertebrates with digits) and near-tetrapods (such as Elpistostege, Tiktaalik, and Panderichthys) from the Devonian period have come from localities in tropical to subtropical paleolatitudes. Most are from Laurussia, a continent incorporating Europe, Greenland, and North America, with only one body fossil and one footprint locality from Australia representing the southern supercontinent Gondwana. Here we describe two previously unknown tetrapods from the Late Devonian (late Famennian) Gondwana locality of Waterloo Farm in South Africa, then located within the Antarctic Circle, which demonstrate that Devonian tetrapods were not restricted to warm environments and suggest that they may have been global in distribution.

Out of Antarctica

Tetrapod Evolution![Figure][1] Tutusius mlambo , a basal tetrapod from the Late Devonian, found in what was then the Antarctic Circle CREDIT: MAGGIE LAMBERT-NEWMAN When we think of Devonian tetrapods, the ancestors of all modern vertebrates, we tend to picture amphibian-like creatures

Engrailed controls epaxial-hypaxial muscle innervation and the establishment of vertebrate three-dimensional mobility

Chordates are characterised by contractile muscle on either side of the body that promotes movement by side-to-side undulation. In the lineage leading to modern jawed vertebrates (crown group gnathostomes), this system was refined: body muscle became segregated into distinct dorsal (epaxial) and ventral (hypaxial) components that are separately innervated by the medial and hypaxial motors column, respectively, via the dorsal and ventral ramus of the spinal nerves. This allows full three-dimensional mobility, which in turn was a key factor in their evolutionary success. How the new gnathostome system is established during embryogenesis and how it may have evolved in the ancestors of modern vertebrates is not known.Vertebrate Engrailed genes have a peculiar expression pattern as they temporarily demarcate a central domain of the developing musculature at the epaxial-hypaxial boundary. Moreover, they are the only genes known with this particular expression pattern. The aim of this study was to investigate whether Engrailed genes control epaxial-hypaxial muscle development and innervation.Investigating chick, mouse and zebrafish as major gnathostome model organisms, we found that the Engrailed expression domain was associated with the establishment of the epaxial-hypaxial boundary of muscle in all three species. Moreover, the outgrowing epaxial and hypaxial nerves orientated themselves with respect to this Engrailed domain. In the chicken, loss and gain of Engrailed function changed epaxial-hypaxial somite patterning. Importantly, in all animals studied, loss and gain of Engrailed function severely disrupted the pathfinding of the spinal motor axons, suggesting that Engrailed plays an evolutionarily conserved role in the separate innervation of vertebrate epaxial-hypaxial muscle.