RESUMO
We use synchrotron x-ray tomography of annual growth increments in the dental cementum of mammaliaforms (stem and crown fossil mammals) from three faunas across the Jurassic to map the origin of patterns of mammalian growth patterns, which are intrinsically related to mammalian endothermy. Although all fossils studied exhibited slower growth rates, longer life spans, and delayed sexual maturity relative to comparably sized extant mammals, the earliest crown mammals developed significantly faster growth rates in early life that reduced at sexual maturity, compared to stem mammaliaforms. Estimation of basal metabolic rates (BMRs) suggests that some fossil crown mammals had BMRs approaching the lowest rates of extant mammals. We suggest that mammalian growth patterns first evolved during their mid-Jurassic adaptive radiation, although growth remained slower than in extant mammals.
Assuntos
Evolução Biológica , Fósseis , Mamíferos , Animais , Cemento Dentário/anatomia & histologia , Síncrotrons , Filogenia , Metabolismo BasalRESUMO
Living mammal groups exhibit rapid juvenile growth with a cessation of growth in adulthood1. Understanding the emergence of this pattern in the earliest mammaliaforms (mammals and their closest extinct relatives) is hindered by a paucity of fossils representing juvenile individuals. We report exceptionally complete juvenile and adult specimens of the Middle Jurassic docodontan Krusatodon, providing anatomical data and insights into the life history of early diverging mammaliaforms. We used synchrotron X-ray micro-computed tomography imaging of cementum growth increments in the teeth2-4 to provide evidence of pace of life in a Mesozoic mammaliaform. The adult was about 7 years and the juvenile 7 to 24 months of age at death and in the process of replacing its deciduous dentition with its final, adult generation. When analysed against a dataset of life history parameters for extant mammals5, the relative sequence of adult tooth eruption was already established in Krusatodon and in the range observed in extant mammals but this development was prolonged, taking place during a longer period as part of a significantly longer maximum lifespan than extant mammals of comparable adult body mass (156 g or less). Our findings suggest that early diverging mammaliaforms did not experience the same life histories as extant small-bodied mammals and the fundamental shift to faster growth over a shorter lifespan may not have taken place in mammaliaforms until during or after the Middle Jurassic.
Assuntos
Fósseis , Mamíferos , Animais , Mamíferos/anatomia & histologia , Microtomografia por Raio-X , Dente/anatomia & histologia , Dente/diagnóstico por imagem , Erupção Dentária/fisiologia , Cemento Dentário/anatomia & histologia , Síncrotrons , Características de História de Vida , História Antiga , Longevidade , FemininoRESUMO
Several families of neogastropod mollusks independently evolved the ability to drill through mineralized prey skeletons using their own mineralized feeding teeth, sometimes with shell-softening chemical agents produced by an organ in the foot. Teeth with more durable tooth shapes should extend their use and improve predator performance, but past studies have described only the cusped-side of teeth, mostly overlooking morphologies related to functional interactions between teeth. Here, we describe the three-dimensional morphology of the central drilling tooth (rachidian) from four species of the neogastropod family Muricidae using synchrotron tomographic microscopy and assemble a three-dimensional model of a multitooth series in drilling position for two of them to investigate their dynamic form. We find two new types of articulating surfaces, including a saddle joint at either end of the rachidian and a large tongue-and-groove joint in the center. The latter has a shape that maximizes contact surface area between teeth as they rotate away from each other during drilling. Articulating joints have not been described in Neogastropod radula previously, but they are consistent with an earlier hypothesis that impact forces on individual teeth during predatory drilling are dispersed by tooth-tooth interactions.
Assuntos
Gastrópodes , Animais , Imageamento Tridimensional , Síncrotrons , Membrana Celular , PéRESUMO
The bone-cartilage unit (BCU) is a universal feature in diarthrodial joints, which is mechanically-graded and subjected to shear and compressive strains. Changes in the BCU have been linked to osteoarthritis (OA) progression. Here we report existence of a physiological internal strain gradient (pre-strain) across the BCU at the ultrastructural scale of the extracellular matrix (ECM) constituents, specifically the collagen fibril. We use X-ray scattering that probes changes in the axial periodicity of fibril-level D-stagger of tropocollagen molecules in the matrix fibrils, as a measure of microscopic pre-strain. We find that mineralized collagen nanofibrils in the calcified plate are in tensile pre-strain relative to the underlying trabecular bone. This behaviour contrasts with the previously accepted notion that fibrillar pre-strain (or D-stagger) in collagenous tissues always reduces with mineralization, via reduced hydration and associated swelling pressure. Within the calcified part of the BCU, a finer-scale gradient in pre-strain (0.6% increase over ~50µm) is observed. The increased fibrillar pre-strain is linked to prior research reporting large tissue-level residual strains under compression. The findings may have biomechanical adaptative significance: higher in-built molecular level resilience/damage resistance to physiological compression, and disruption of the molecular-level pre-strains during remodelling of the bone-cartilage interface may be potential factors in osteoarthritis-based degeneration.
Assuntos
Osteoartrite , Tropocolágeno , Cartilagem , Colágeno/química , Matriz Extracelular , HumanosRESUMO
We suggest that mammalian endothermy was established amongst Middle Jurassic crown mammals, through reviewing state-of-the-art fossil and living mammal studies. This is considerably later than the prevailing paradigm, and has important ramifications for the causes, pattern, and pace of physiological evolution amongst synapsids. Most hypotheses argue that selection for either enhanced aerobic activity, or thermoregulation was the primary driver for synapsid physiological evolution, based on a range of fossil characters that have been linked to endothermy. We argue that, rather than either alternative being the primary selective force for the entirety of endothermic evolution, these characters evolved quite independently through time, and across the mammal family tree, principally as a response to shifting environmental pressures and ecological opportunities. Our interpretations can be tested using closely linked proxies for both factors, derived from study of fossils of a range of Jurassic and Cretaceous mammaliaforms and early mammals.
Assuntos
Evolução Biológica , Mamíferos , Animais , Fósseis , Mamíferos/fisiologia , FilogeniaRESUMO
BACKGROUND: Scales are mineralised exoskeletal structures that are part of the dermal skeleton. Scales have been mostly lost during evolution of terrestrial vertebrates whilst bony fish have retained a mineralised dermal skeleton in the form of fin rays and scales. Each scale is a mineralised collagen plate that is decorated with both matrix-building and resorbing cells. When removed, an ontogenetic scale is quickly replaced following differentiation of the scale pocket-lining cells that regenerate a scale. Processes promoting de novo matrix formation and mineralisation initiated during scale regeneration are poorly understood. Therefore, we performed transcriptomic analysis to determine gene networks and their pathways involved in dermal scale regeneration. RESULTS: We defined the transcriptomic profiles of ontogenetic and regenerating scales of zebrafish and identified 604 differentially expressed genes (DEGs). These were enriched for extracellular matrix, ossification, and cell adhesion pathways, but not in enamel or dentin formation processes indicating that scales are reminiscent to bone. Hypergeometric tests involving monogenetic skeletal disorders showed that DEGs were strongly enriched for human orthologues that are mutated in low bone mass and abnormal bone mineralisation diseases (P< 2× 10-3). The DEGs were also enriched for human orthologues associated with polygenetic skeletal traits, including height (P< 6× 10-4), and estimated bone mineral density (eBMD, P< 2× 10-5). Zebrafish mutants of two human orthologues that were robustly associated with height (COL11A2, P=6× 10-24) or eBMD (SPP1, P=6× 10-20) showed both exo- and endo- skeletal abnormalities as predicted by our genetic association analyses; col11a2Y228X/Y228X mutants showed exoskeletal and endoskeletal features consistent with abnormal growth, whereas spp1P160X/P160X mutants predominantly showed mineralisation defects. CONCLUSION: We show that scales have a strong osteogenic expression profile comparable to other elements of the dermal skeleton, enriched in genes that favour collagen matrix growth. Despite the many differences between scale and endoskeletal developmental processes, we also show that zebrafish scales express an evolutionarily conserved sub-population of genes that are relevant to human skeletal disease.
Assuntos
Proteínas de Peixe-Zebra , Peixe-Zebra , Animais , Perfilação da Expressão Gênica , Humanos , Peixe-Zebra/metabolismo , Proteínas de Peixe-Zebra/genética , Proteínas de Peixe-Zebra/metabolismoRESUMO
Cementum, the tissue attaching mammal tooth roots to the periodontal ligament, grows appositionally throughout life, displaying a series of circum-annual incremental features. These have been studied for decades as a direct record of chronological lifespan. The majority of previous studies on cementum have used traditional thin-section histological methods to image and analyse increments. However, several caveats have been raised in terms of studying cementum increments in thin-sections. Firstly, the limited number of thin-sections and the two-dimensional perspective they impart provide an incomplete interpretation of cementum structure, and studies often struggle or fail to overcome complications in increment patterns that complicate or inhibit increment counting. Increments have been repeatedly shown to both split and coalesce, creating accessory increments that can bias increment counts. Secondly, identification and counting of cementum increments using human vision is subjective, and it has led to inaccurate readings in several experiments studying individuals of known age. Here, we have attempted to optimise a recently introduced imaging modality for cementum imaging; X-ray propagation-based phase-contrast imaging (PPCI). X-ray PPCI was performed for a sample of rhesus macaque (Macaca mulatta) lower first molars (n = 10) from a laboratory population of known age. PPCI allowed the qualitative identification of primary/annual versus intermittent secondary increments formed by splitting/coalescence. A new method for semi-automatic increment counting was then integrated into a purpose-built software package for studying cementum increments, to count increments in regions with minimal complications. Qualitative comparison with data from conventional cementochronology, based on histological examination of tissue thin-sections, confirmed that X-ray PPCI reliably and non-destructively records cementum increments (given the appropriate preparation of specimens prior to X-ray imaging). Validation of the increment counting algorithm suggests that it is robust and provides accurate estimates of increment counts. In summary, we show that our new increment counting method has the potential to overcome caveats of conventional cementochronology approaches, when used to analyse three-dimensional images provided by X-ray PPCI.
Assuntos
Algoritmos , Cemento Dentário/diagnóstico por imagem , Dente Molar/diagnóstico por imagem , Síncrotrons , Tomografia Computadorizada por Raios X , Animais , Macaca mulattaRESUMO
Bone homeostasis is a dynamic, multicellular process that is required throughout life to maintain bone integrity, prevent fracture, and respond to skeletal damage. WNT16 has been linked to bone fragility and osteoporosis in human genome wide-association studies, as well as the functional hematopoiesis of leukocytes in vivo. However, the mechanisms by which WNT16 promotes bone health and repair are not fully understood. In this study, CRISPR-Cas9 was used to generate mutant zebrafish lacking Wnt16 (wnt16 -/- ) to study its effect on bone dynamically. The wnt16 mutants displayed variable tissue mineral density (TMD) and were susceptible to spontaneous fractures and the accumulation of bone calluses at an early age. Fractures were induced in the lepidotrichia of the caudal fins of wnt16 -/- and WT zebrafish; this model was used to probe the mechanisms by which Wnt16 regulates skeletal and immune cell dynamics in vivo. In WT fins, wnt16 expression increased significantly during the early stages for bone repair. Mineralization of bone during fracture repair was significantly delayed in wnt16 mutants compared with WT zebrafish. Surprisingly, there was no evidence that the recruitment of innate immune cells to fractures or soft callus formation was altered in wnt16 mutants. However, osteoblast recruitment was significantly delayed in wnt16 mutants postfracture, coinciding with precocious activation of the canonical Wnt signaling pathway. In situ hybridization suggests that canonical Wnt-responsive cells within fractures are osteoblast progenitors, and that osteoblast differentiation during bone repair is coordinated by the dynamic expression of runx2a and wnt16. This study highlights zebrafish as an emerging model for functionally validating osteoporosis-associated genes and investigating fracture repair dynamically in vivo. Using this model, it was found that Wnt16 protects against fracture and supports bone repair, likely by modulating canonical Wnt activity via runx2a to facilitate osteoblast differentiation and bone matrix deposition. © 2021 The Authors. JBMR Plus published by Wiley Periodicals LLC. on behalf of American Society for Bone and Mineral Research.
RESUMO
Cementum is a mineralized dental tissue common to mammals that grows throughout life, following a seasonally appositional rhythm. Each year, one thick translucent increment and one thin opaque increment is deposited, offering a near-complete record of an animal's life history. Male and female mammals exhibit significant differences in oral health, due to the contrasting effects of female versus male sex hormones. Oestrogen and progesterone have a range of negative effects on oral health that extends to the periodontium and cementum growth interface. Here, we use synchrotron radiation-based X-ray tomography to image the cementum of a sample of rhesus macaque (Macaca mulatta) teeth from individuals of known life history. We found that increased breeding history in females corresponds with increased increment tortuosity and less organized cementum structure, when compared to male and juvenile cementum. We quantified structural differences by measuring the greyscale 'texture' of cementum and comparing results using principal components analysis. Adult females and males occupy discrete regions of texture space with no overlap. Females with known pregnancy records also have significantly different cementum when compared with non-breeding and juvenile females. We conclude that several aspects of cementum structure and texture may reflect differences in sexual life history in primates.
Assuntos
Síncrotrons , Dente , Animais , Cemento Dentário/diagnóstico por imagem , Feminino , Macaca mulatta , Masculino , Tomografia por Raios XRESUMO
Despite considerable advances in knowledge of the anatomy, ecology and evolution of early mammals, far less is known about their physiology. Evidence is contradictory concerning the timing and fossil groups in which mammalian endothermy arose. To determine the state of metabolic evolution in two of the earliest stem-mammals, the Early Jurassic Morganucodon and Kuehneotherium, we use separate proxies for basal and maximum metabolic rate. Here we report, using synchrotron X-ray tomographic imaging of incremental tooth cementum, that they had maximum lifespans considerably longer than comparably sized living mammals, but similar to those of reptiles, and so they likely had reptilian-level basal metabolic rates. Measurements of femoral nutrient foramina show Morganucodon had blood flow rates intermediate between living mammals and reptiles, suggesting maximum metabolic rates increased evolutionarily before basal metabolic rates. Stem mammals lacked the elevated endothermic metabolism of living mammals, highlighting the mosaic nature of mammalian physiological evolution.
Assuntos
Mamíferos/fisiologia , Répteis/fisiologia , Animais , Metabolismo Basal , Evolução Biológica , Fósseis/anatomia & histologia , Fósseis/história , História Antiga , Mamíferos/classificação , Filogenia , Tomografia por Raios X , Dente/anatomia & histologia , Dente/químicaRESUMO
Scoliosis is an abnormal bending of the body axis. Truncated vertebrae or a debilitated ability to control the musculature in the back can cause this condition, but in most cases the causative reason for scoliosis is unknown (idiopathic). Using mutants for somite clock genes with mild defects in the vertebral column, we here show that early defects in somitogenesis are not overcome during development and have long lasting and profound consequences for muscle fiber organization, structure and whole muscle volume. These mutants present only mild alterations in the vertebral column, and muscle shortcomings are uncoupled from skeletal defects. None of the mutants presents an overt musculoskeletal phenotype at larval or early adult stages, presumably due to compensatory growth mechanisms. Scoliosis becomes only apparent during aging. We conclude that adult degenerative scoliosis is due to disturbed crosstalk between vertebrae and muscles during early development, resulting in subsequent adult muscle weakness and bending of the body axis.
RESUMO
The spine is the central skeletal support structure in vertebrates consisting of repeated units of bone, the vertebrae, separated by intervertebral discs (IVDs) that enable the movement of the spine. Spinal pathologies such as idiopathic back pain, vertebral compression fractures and IVD failure affect millions of people worldwide. Animal models can help us to understand the disease process, and zebrafish are increasingly used as they are highly genetically tractable, their spines are axially loaded like humans, and they show similar pathologies to humans during ageing. However, biomechanical models for the zebrafish are largely lacking. Here, we describe the results of loading intact zebrafish spinal motion segments on a material testing stage within a micro-computed tomography machine. We show that vertebrae and their arches show predictable patterns of deformation prior to their ultimate failure, in a pattern dependent on their position within the segment. We further show using geometric morphometrics which regions of the vertebra deform the most during loading, and that finite-element models of the trunk subjected reflect the real patterns of deformation and strain seen during loading and can therefore be used as a predictive model for biomechanical performance.
Assuntos
Envelhecimento/metabolismo , Disco Intervertebral/metabolismo , Movimento , Peixe-Zebra/metabolismo , Envelhecimento/patologia , Animais , Dor nas Costas/metabolismo , Dor nas Costas/patologia , Modelos Animais de Doenças , Análise de Elementos Finitos , Humanos , Disco Intervertebral/patologia , Suporte de CargaRESUMO
The discovery of large, complex, internal canals within the rostra of fossil reptiles has been linked with an enhanced tactile function utilised in an aquatic context, so far in pliosaurids, the Cretaceous theropod Spinosaurus, and the related spinosaurid Baryonyx. Here, we report the presence of a complex network of large, laterally situated, anastomosing channels, discovered via micro-focus computed tomography (µCT), in the premaxilla and maxilla of Neovenator, a mid-sized allosauroid theropod from the Early Cretaceous of the UK. We identify these channels as neurovascular canals, that include parts of the trigeminal nerve; many branches of this complex terminate on the external surfaces of the premaxilla and maxilla where they are associated with foramina. Neovenator is universally regarded as a 'typical' terrestrial, predatory theropod, and there are no indications that it was aquatic, amphibious, or unusual with respect to the ecology or behaviour predicted for allosauroids. Accordingly, we propose that enlarged neurovascular facial canals shouldn't be used to exclusively support a model of aquatic foraging in theropods and argue instead that an enhanced degree of facial sensitivity may have been linked with any number of alternative behavioural adaptations, among them defleshing behaviour, nest selection/maintenance or social interaction.