Revisiting the links between bone remodelling and osteocytes: insights from across phyla

We question two major tenets of bone biology: that the primary role of remodelling is to remove damage in the bone (so‐called damage‐driven remodelling) and that osteocytes are the only strain‐sensing orchestrators of this process. These concepts are distilled largely from research on model mammal species, but in fact, there are a number of features of various bones, from mammalian and non‐mammalian species, that do not accord with these ‘rules’. Here, we assemble a variety of examples, ranging from species that lack osteocytes but that still seem capable of remodelling their bones, to species with osteocytic bones that do not remodel, and to instances of inter‐species, inter‐bone and/or intra‐bone variation in bone remodelling that show that this purported repair process is not always where the ‘rules’ tell us it should be. This collection of points argues that our understanding of the advantages, roles and primary drivers of remodelling are inadequate and biased to quite a small phylogenetic cross section of the species that possess bone. We suggest a variety of new directions for bone research that would provide us with a better understanding of bone remodelling, tying together the interests of comparative biologists, palaeontologists and medical researchers.     

Micromorphological,geochemical, and diagenetic characterization of sirenian ribs preserved in the Late Miocene paleontological site of Cessaniti (southern Calabria,Italy)

The site of Cessaniti (Vibo Valentia, Italy) has been well known since the 19th century for the richness and good preservation of its Miocene fauna and flora. The sedimentary succession of the site represents a paralic system that evolved toward an open-marine environment recording the Tortonian transgression. The fossil assemblage contains rich invertebrate (corals, bivalves, gastropods, brachiopods, echinoids, benthic and planktonic foraminifers) and vertebrate faunas (proboscideans, rhinoceroses, giraffids, bovids, sirenids, marine turtles, and fish remains). The fossils recovered at the Cessaniti site have a relevant role in phylogenetic studies and paleogeographic reconstructions of Late Miocene environments of the southern Italy. This research is focused on the microstructure and preservation state of the fossil bones. Samples of Metaxytherium sp. bones have been analyzed to understand the diagenetic profile of the bone assemblages that characterizes the taphonomic history of the Cessaniti site. The analyses provided a comprehensive account of how bone mineral (bioapatite) has been altered and demonstrated that the post-burial processes did not significantly affect the micromorphological and biogeochemical features of the bones. The excellent preservation state of the bones strengthens the importance of the Cessaniti site for studies of the Mediterranean Miocene vertebrate fauna.     

Rietveld refinement on x-ray diffraction patterns of bioapatite in human fetal bones

Bioapatite, the main constituent of mineralized tissue in mammalian bones, is a calcium-phosphate-based mineral that is similar in structure and composition to hydroxyapatite. In this work, the crystallographic structure of bioapatite in human fetuses was investigated by synchrotron radiation x-ray diffraction (XRD) and microdiffraction ( micro -XRD) techniques. Rietveld refinement analyses of XRD and micro -XRD data allow for quantitative probing of the structural modifications of bioapatite as functions of the mineralization process and gestational age.     

Palaeomorphology: fossils and the inference of cladistic relationships

Edgecombe, G.D. 2010. Palaeomorphology: fossils and the inference of cladistic relationships. —Acta Zoologica (Stockholm) 91 : 72–80 Twenty years have passed since it was empirically demonstrated that inclusion of extinct taxa could overturn a phylogenetic hypothesis formulated upon extant taxa alone, challenging Colin Patterson’s bold conjecture that this phenomenon ‘may be non‐existent’. Suppositions and misconceptions about missing data, often couched in terms of ‘wildcard taxa’ and ‘the missing data problem’, continue to cloud the literature on the topic of fossils and phylogenetics. Comparisons of real data sets show that no a priori (or indeed a posteriori) decisions can be made about amounts of missing data and most properties of cladograms, and both simulated and real data sets demonstrate that even highly incomplete taxa can impact on relationships. The exclusion of fossils from phylogenetic analyses is neither theoretically nor empirically defensible.     

Cranial base morphology and temporal bone pneumatization in Asian Homo erectus

The external morphological features of the temporal bone are used frequently to determine taxonomic affinities of fossils of the genus Homo. Temporal bone pneumatization has been widely studied in great apes and in early hominids. However, this feature is rarely examined in the later hominids, particularly in Asian Homo erectus. We provide a comparative morphological and quantitative analysis of Asian Homo erectus from the sites of Ngandong, Sambungmacan, and Zhoukoudian, and of Neandertals and anatomically modern Homo sapiens in order to discuss causes and modalities of temporal bone pneumatization during hominid evolution. The evolution of temporal bone pneumatization in the genus Homo is more complex than previously described. Indeed, the Zhoukoudian fossils have a unique pattern of temporal bone pneumatization, whereas Ngandong and Sambungmacan fossils, as well as the Neandertals, more closely resemble the modern human pattern. Moreover, these Chinese fossils are characterized by a wide midvault and a relatively narrow occipital bone. Our results support the point of view that cell development does not play an active role in determining cranial base morphology. Instead, pneumatization is related to available space and to temporal bone morphology, and its development is related to correlated morphology and the relative disposition of the bones and cerebral lobes. Because variation in pneumatization is extensive within the same species, the phyletic implications of pneumatization are limited in the taxa considered here.     

The occipital region in the basal bony fish Erpetoichthys calabaricus (Actinopterygii: Cladistia)

Erpetoichthys calabaricus has unusual cranio‐vertebral anatomy, with an occipital centrum forming a component part of the compound basiexoccipital bone, and a ‘free‐floating’ occipital neural arch that differs from accessory arches found in some teleosts. The occipital neural arch bears autapomorphic lateral projections that articulate with small rod‐like bones resembling the spatial relationship of parapophyses and ribs, a feature normally restricted to vertebral centra. Based on analyses of cleared and stained specimens, computed tomography and histology, it is hypothesized that the lateral projections and associated rod‐shaped bones are structures that share developmental homologies to the unique ‘dorsal ribs’ of Polypteridae.     

Effect of bone mineral density on masticatory performance and efficiency

doi: 10.1111/j.1741‐2358.2010.00414.x Effect of bone mineral density on masticatory performance and efficiency Objective: To evaluate the effect of bone mineral density (BMD) on masticatory performance and efficiency in dentate subjects. Background data: Osteoporosis is the most common disorder of the bone. It causes reduction in BMD of the all the skeletal tissue including jaw bones. It also promotes bone loss in jaw bones. In osteoporosis, a reduction of maximal bite force and greater electromyography activity of masticatory muscles is documented. This may lead to the development of masticatory dysfunction which can be assessed by a chewing test in the form of change in masticatory performance and efficiency. Materials and methods: Sixty subjects with equal numbers of men and women were selected for the study, in which BMD screening (T‐score) was carried out to identify the normal, osteopenic and osteoporotic subjects. Their masticatory performance and efficiency was evaluated by a chewing test (fractional sieving method). Results: A high ‘T’ score was associated with low masticatory efficiency and a low ‘T’ score with high masticatory efficiency. Masticatory performance and efficiency was significantly higher among males as compared to females with similar range of BMD. Conclusion: In both genders, high BMD groups (low ‘T’ score) had a significantly high percentage of masticatory efficiency compared to the low BMD (high ‘T’ score) group.     

Taphonomy of the reference Miocene vertebrate mammal site of Cerro de la Garita,Spain

This article reports a detailed taphonomic study of the reference Miocene vertebrate site of Cerro de la Garita, (Concud, Teruel, Spain). The sedimentary record of the site indicates that it was a palaeo‐lakeshore, and this conclusion is supported by aquatic environment‐related taphonomic modifications of its fossils (both on their surfaces and internally). The site provided a water source that appears to have been regularly visited by herbivores. It was, therefore, also likely to have been a good feeding ground for predators and scavengers. Hyaena coprolites have been found at the site, and tooth marks were identified on some fossil bone surfaces. Bone fragments 2–5 cm in length showed clear evidence of heavy digestion and probable regurgitation. Abundant trampling marks were seen on the surface of many of the fossil bones, traits that are congruent with a damp lakeshore environment. Most of the remains were broken, and only a few anatomical elements belonging to the same individual were found close together, although never articulated (i.e. in a manner reflecting their anatomical connections). The fossils showed no signs of selection (either by shape or size) or abrasion, although a certain re‐orientation suggests the influence of wave or strand line activity. Despite being an open‐air site, none of the fossils appeared to be weathered, further suggesting that the surrounding environment was a damp lakeshore probably shaded by vegetation. Indeed, abundant signs of root activity were observed. No evidence of reworking, that is, post‐burial disturbance or diachronic mixing of fossils, was seen, confirming the international value of Cerro de la Garita as a reference site for continental Miocene mammal assemblages.     

Scaling of Haversian canal surface area to secondary osteon bone volume in ribs and limb bones

Studies of secondary osteons in ribs have provided a great deal of what is known about remodeling dynamics. Compared with limb bones, ribs are metabolically more active and sensitive to hormonal changes, and receive frequent low‐strain loading. Optimization for calcium exchange in rib osteons might be achieved without incurring a significant reduction in safety factor by disproportionally increasing central canal size with increased osteon size (positive allometry). By contrast, greater mechanical loads on limb bones might favor reducing deleterious consequences of intracortical porosity by decreasing osteon canal size with increased osteon size (negative allometry). Evidence of this metabolic/mechanical dichotomy between ribs and limb bones was sought by examining relationships between Haversian canal surface area (BS, osteon Haversian canal perimeter, HC.Pm) and bone volume (BV, osteonal wall area, B.Ar) in a broad size range of mature (quiescent) osteons from adult human limb bones and ribs (modern and medieval) and various adult and subadult non‐human limb bones and ribs. Reduced major axis (RMA) and least‐squares (LS) regressions of HC.Pm/B.Ar data show that rib and limb osteons cannot be distinguished by dimensional allometry of these parameters. Although four of the five rib groups showed positive allometry in terms of the RMA slopes, nearly 50% of the adult limb bone groups also showed positive allometry when negative allometry was expected. Consequently, our results fail to provide clear evidence that BS/BV scaling reflects a rib versus limb bone dichotomy whereby calcium exchange might be preferentially enhanced in rib osteons. Am J Phys Anthropol 151:230–244, 2013. © 2013 Wiley Periodicals, Inc.     

Hominin first metatarsals (SKX 5017 and SK 1813) from Swartkrans: a morphometric analysis.

Two hominin metatarsals from Swartkrans, SKX 5017 and SK 1813, have been reported by Susman and Brain [1988. New first metatarsal (SKX 5017) from Swartkrans and the gait of Paranthropus robustus. Am. J. Phys. Anthropol. 79, 451-454] and Susman and de Ruiter [2004. New hominin first metatarsal (SK 1813) from Swartkrans. J. Hum. Evol. 47, 171-181]. They found these bones to have both primitive and derived traits indicating that, while being bipedal, these hominines had a unique toe-off mechanism. We have undertaken additional multivariate morphometric analyses, comparing the fossils to the first metatarsals of modern humans and extant apes. The largest proportion of discrimination lies in the different locomotor functions: apes on the one hand and the humans and fossils on the other. While the fossils have the closest affinity to humans, they have a unique biomechanical pattern suggesting a more facultative form of bipedalism. The implications of this are, while morphometric analyses do not necessarily directly capture the described primitive and derived traits, the associated functional pattern is held within the broader morphology of the bone.     

A tale of two cities: The genetic mechanisms governing calvarial bone development

The skull bones must grow in a coordinated, three‐dimensional manner to coalesce and form the head and face. Mammalian skull bones have a dual embryonic origin from cranial neural crest cells (CNCC) and paraxial mesoderm (PM) and ossify through intramembranous ossification. The calvarial bones, the bones of the cranium which cover the brain, are derived from the supraorbital arch (SOA) region mesenchyme. The SOA is the site of frontal and parietal bone morphogenesis and primary center of ossification. The objective of this review is to frame our current in vivo understanding of the morphogenesis of the calvarial bones and the gene networks regulating calvarial bone initiation in the SOA mesenchyme.     

Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation

We present novel findings on sauropod bone histology that cast doubt on general palaeohistological concepts concerning the true nature of woven bone in primary cortical bone and its role in the rapid growth and giant body sizes of sauropod dinosaurs. By preparing and investigating longitudinal thin sections of sauropod long bones, of which transverse thin sections were published previously, we found that the amount of woven bone in the primary complex has been largely overestimated. Using comparative cellular and light‐extinction characteristics in the two section planes, we revealed that the majority of the bony lamina consists of longitudinally organized primary bone, whereas woven bone is usually represented only by a layer a few cells thin in the laminae. Previous arguments on sauropod biology, which have been based on the overestimated amount, misinterpreted formation process and misjudged role of woven bone in the plexiform bone formation of sauropod dinosaurs, are thereby rejected. To explain the observed pattern in fossil bones, we review the most recent advances in bone biology concerning bone formation processes at the cellular and tissue levels. Differentiation between static and dynamic osteogenesis (SO and DO) and the revealed characteristics of SO‐ versus DO‐derived bone tissues shed light on several questions raised by our palaeohistological results and permit identification of these bone tissues in fossils with high confidence. By presenting the methods generally used for investigating fossil bones, we show that the major cause of overestimation of the amount of woven bone in previous palaeohistological studies is the almost exclusive usage of transverse sections. In these sections, cells and crystallites of the longitudinally organized primary bone are cut transversely, thus cells appear rounded and crystallites remain dark under crossed plane polarizers, thereby giving the false impression of woven bone. In order to avoid further confusion in palaeohistological studies, we introduce new osteohistological terms as well as revise widely used but incorrect terminology. To infer the role of woven bone in the bone formation of fast‐growing tetrapods, we review some aspects of the interrelationships between the vascularity of bone tissues, basal metabolic rate, body size and growth rate. By putting our findings into the context of osteogenesis, we provide a new model for the diametrical limb bone growth of sauropods and present new implications for the evolution of fast growth in vertebrates. Since biomechanical studies of bone tissues suggest that predominant collagen fibre orientation (CFO) is controlled by endogenous, functional and perhaps phylogenetic factors, the relationship between CFO and bone growth rate as defined by Amprino's rule, which has been the basis for the biological interpretation of several osteohistological features, must be revised. Our findings draw attention to the urgent need for revising widely accepted basic concepts of palaeohistological studies, and for a more integrative approach to bone formation, biomechanics and bone microstructural features of extant and extinct vertebrates to infer life history traits of long extinct, iconic animals like dinosaurs.     

Bony‐toothed birds (Aves: Pelagornithidae) from the Middle Eocene of Belgium

Abstract: We describe well‐preserved remains of the Pelagornithidae (bony‐toothed birds) from the middle Eocene of Belgium, including a sternum, pectoral girdle bones and humeri of a single individual. The specimens are tentatively assigned to Macrodontopteryx oweni Harrison and Walker, 1976 , which has so far only been known from the holotype skull and a referred proximal ulna. Another species, about two times larger, is represented by an incomplete humerus and tentatively identified as Dasornis emuinus ( Bowerbank, 1854 ). The fossils provide critical new data on the osteology of the pectoral girdle of bony‐toothed birds. For the first time, the sternum of one of the smaller species is preserved, and this bone exhibits a more plesiomorphic morphology than the recently described sternum of the giant Miocene taxon Pelagornis. The coracoid resembles that of the Diomedeidae (albatrosses) in overall morphology, but because bony‐toothed birds lack apomorphies of the Procellariiformes, the similarities are almost certainly owing to convergence. Bony‐toothed birds were often compared with the ‘Pelecaniformes’ by previous authors, who especially made comparisons with the Sulidae (gannets and boobies). However, the coracoid distinctly differs from that of extant ‘pelecaniform’ birds, and the plesiomorphic presence of a foramen nervi supracoracoidei as well as the absence of a well‐delimited articulation facet for the furcula supports a position outside the Suloidea, the clade to which the Sulidae belong.     

Muscle‐induced loading as an important source of variation in craniofacial skeletal shape

The shape of the craniofacial skeleton is constantly changing through ontogeny and reflects a balance between developmental patterning and mechanical‐load‐induced remodeling. Muscles are a major contributor to producing the mechanical environment that is crucial for “normal” skull development. Here, we use an F₅ hybrid population of Lake Malawi cichlids to characterize the strength and types of associations between craniofacial bones and muscles. We focus on four bones/bone complexes, with different developmental origins, alongside four muscles with distinct functions. We used micro‐computed tomography to extract 3D information on bones and muscles. 3D geometric morphometrics and volumetric measurements were used to characterize bone and muscle shape, respectively. Linear regressions were performed to test for associations between bone shape and muscle volume. We identified three types of associations between muscles and bones: weak, strong direct (i.e., muscles insert directly onto bone), and strong indirect (i.e., bone is influenced by muscles without a direct connection). In addition, we show that although the shape of some bones is relatively robust to muscle‐induced mechanical stimulus, others appear to be highly sensitive to muscular input. Our results imply that the roles for muscular input on skeletal shape extend beyond specific points of origin or insertion and hold significant potential to influence broader patterns of craniofacial geometry. Thus, changes in the loading environment, either as a normal course of ontogeny or if an organism is exposed to a novel environment, may have pronounced effects on skeletal shape via near and far‐ranging effects of muscular loading.     

Differentiation and growth of bone ornamentation in vertebrates: A comparative histological study among the Crocodylomorpha

Bone ornamentation, that is, hollow (pits and grooves) or protruding (ridges) repetitive reliefs on the surface of dermal bones, is a frequent, though poorly studied and understood, feature in vertebrates. One of the most typical examples of this characteristic is given by the Crurotarsi, a taxon formed by the crocodilians and their closest allies, which generally display deep ornamentation on skull roof and osteoderms. However, the ontogenetic process responsible for the differentiation and development of this character remains controversial. This study was conducted to settle the question on histological and microanatomical evidence in several crurotarsan taxa. Observational and experimental data in extant and extinct crocodyliforms show that bone ornamentation is initially created, and later maintained during somatic growth (that is indefinite in crocodilians), by a complex process of bone remodeling comprising local resorption of superficial bone cortices, followed by partial reconstruction. The superficial reliefs of crocodilian dermal bones are thus permanently modified through pit enlargement, drift, stretching, shrinking, or complete filling. Ridges are also remodeled in corresponding ways. These processes allow accommodation of unitary ornamental motifs to the overall dimensions of the bones during growth. A parsimony optimization based on the results of this study, but integrating also published data on bone histology in non‐crocodyliform crurotarsans and some non‐crurotarsan taxa, suggests that the peculiar mechanism described above for creating and maintaining bone ornamentation is a general feature of the Crurotarsi and is quite distinct from that attributed by previous authors to other vertebrates. J. Morphol. 276:425–445, 2015. © 2014 Wiley Periodicals, Inc.     

Intravascular microstructures in trabecular bone tissues of Tyrannosaurus rex

Histological analyses of trabecular tissue from the limb bones of a Tyrannosaurus rex revealed the presence of small (average 25 μm) round microstructures in the vascular channels of the bone. These bony tissues otherwise evidenced minimal diagenetic change, and no secondary mineral deposition was observed in the vessel channels. While we have published analyses of the bony tissues of this specimen, we have not published data obtained on these small intravascular microstructures. Several characteristics link these microstructures to endogenous biological components, although their origin is not confirmed, and several hypotheses are considered. A discussion of the meaning of the term ‘organic preservation’ and a suggestion of criteria that should be met to be described as such is included.     

The utility of osteon shape and circularity for differentiating human and non-human Haversian bone

Distinguishing human from non‐human bone fragments is usually accomplished by observation of gross morphology. When macroscopic analysis is insufficient, histological approaches can be applied. Microscopic features, like plexiform bone or osteon banding, are characteristic of non‐humans. In the absence of such features, distinguishing Haversian bone as either human or non‐human proves problematic. This study proposes a histomorphometric approach for classifying species from Haversian bone. Two variables, osteon area (On.Ar.) and circularity (On.Cr.), are examined. Measurements were collected from three species (deer, dog, human) represented by various skeletal elements; only ribs were available for humans (ribs: deer n = 6, dog n = 6, human n = 26; humeri: deer n = 6, dog n = 6; femora: deer n = 6, dog n = 6). Qualitative analysis comparing human to non‐human On.Ar. demonstrated that human ribs have larger mean On.Ar. (0.036 mm²) than non‐human ribs (deer = 0.017 mm², dog = 0.013 mm²). On.Cr. in the ribs showed minor differences between species (deer = 0.877; dog = 0.885; human = 0.898). Results demonstrated no significant difference across long bone quadrants in long bones. Discriminant analyses run on the means for each sample demonstrated overlap in deer and dog samples, clustering the non‐human and human groups apart from each other. Mean On.Cr. proved a poor criterion (ribs only: 76.3%, pooled elements: 66.1%), while mean On.Ar. proved useful in identifying human from non‐human samples (ribs only: 92.1%, pooled elements: 93.5%). When variables were combined, accuracy increased to 100% correct classification for rib data and 98.4% when considering data from all elements. These results indicate that On.Ar. and On.Cr. are valuable histomorphometric tools for distinguishing human from non‐human Haversian bone. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.