The ‘biomineralization toolkit’ and the origin of animal skeletons

Biomineralized skeletons are widespread in animals, and their origins can be traced to the latest Ediacaran or early Cambrian fossil record, in virtually all animal groups. The origin of animal skeletons is inextricably linked with the diversification of animal body plans and the dramatic changes in ecology and geosphere–biosphere interactions across the Ediacaran–Cambrian transition. This apparent independent acquisition of skeletons across diverse animal clades has been proposed to have been driven by co‐option of a conserved ancestral genetic toolkit in different lineages at the same time. This ‘biomineralization toolkit’ hypothesis makes predictions of the early evolution of the skeleton, predictions tested herein through a critical review of the evidence from both the fossil record and development of skeletons in extant organisms. Furthermore, the distribution of skeletons is here plotted against a time‐calibrated animal phylogeny, and the nature of the deep ancestors of biomineralizing animals interpolated using ancestral state reconstruction. All these lines of evidence point towards multiple instances of the evolution of biomineralization through the co‐option of an inherited organic skeleton and genetic toolkit followed by the stepwise acquisition of more complex skeletal tissues under tighter biological control. This not only supports the ‘biomineralization toolkit’ hypothesis but also provides a model for describing the evolution of complex biological systems across the Ediacaran–Cambrian transition.     

Regularity in irregular echinoids

 Using the mathematical concept of eutactic star, we prove that it is possible to define a morphospace for irregular echinoids by using a single parameter. In particular, we have found an extraordinary geometric property in the flower-like patterns of the five ambulacral petals of these animals. This property is fulfilled with great accuracy for a large collection of fossil specimens and provides new insights in the study of the viable skeletal designs of extinct and/or living organisms. Received: 19 June 2001 / Revised version: 2 October 2001 / Published online: 14 March 2002     

Physical modelling in biomechanics

Physical models, like mathematical models, are useful tools in biomechanical research. Physical models enable investigators to explore parameter space in a way that is not possible using a comparative approach with living organisms: parameters can be varied one at a time to measure the performance consequences of each, while values and combinations not found in nature can be tested. Experiments using physical models in the laboratory or field can circumvent problems posed by uncooperative or endangered organisms. Physical models also permit some aspects of the biomechanical performance of extinct organisms to be measured. Use of properly scaled physical models allows detailed physical measurements to be made for organisms that are too small or fast to be easily studied directly. The process of physical modelling and the advantages and limitations of this approach are illustrated using examples from our research on hydrodynamic forces on sessile organisms, mechanics of hydraulic skeletons, food capture by zooplankton and odour interception by olfactory antennules.     

How corals made rocks through the ages

Hard, or stony, corals make rocks that can, on geological time scales, lead to the formation of massive reefs in shallow tropical and subtropical seas. In both historical and contemporary oceans, reef‐building corals retain information about the marine environment in their skeletons, which is an organic–inorganic composite material. The elemental and isotopic composition of their skeletons is frequently used to reconstruct the environmental history of Earth's oceans over time, including temperature, pH, and salinity. Interpretation of this information requires knowledge of how the organisms formed their skeletons. The basic mechanism of formation of calcium carbonate skeleton in stony corals has been studied for decades. While some researchers consider coral skeletons as mainly passive recorders of ocean conditions, it has become increasingly clear that biological processes play key roles in the biomineralization mechanism. Understanding the role of the animal in living stony coral biomineralization and how it evolved has profound implications for interpreting environmental signatures in fossil corals to understand past ocean conditions. Here we review historical hypotheses and discuss the present understanding of how corals evolved and how their skeletons changed over geological time. We specifically explain how biological processes, particularly those occurring at the subcellular level, critically control the formation of calcium carbonate structures. We examine the different models that address the current debate including the tissue–skeleton interface, skeletal organic matrix, and biomineralization pathways. Finally, we consider how understanding the biological control of coral biomineralization is critical to informing future models of coral vulnerability to inevitable global change, particularly increasing ocean acidification.     

Estimating body weight and habitat type from extinct avian and avian‐like theropod footprints

The relationship between body weight and footprint area of modern avians was derived and used to estimate the body weights of non‐avian theropods taxa from the Triassic to Cretaceous and extinct avian taxa from the Cretaceous periods. Geometric information, such as the area and shape of fossil tracks of extinct avians and non‐avian theropods, was used to estimate body weight and habitat type. The percentage prediction and standard error of estimates indicated that the body weight estimated from track area is comparable with body weight estimated from body fossils bones. Therefore, this approach is useful when the fossilized track record is richer than the fossilized skeletal record. The data sets for avians and reptiles were combined and used to derive a body weight–area relationship that may be applicable to a broader range of organisms, such as plantigrade quadrupeds and digitigrade bipeds. Additionally, scatter plots of the relationship between habitat type and footprint shape of modern avians were used to infer the habitat type of extinct avians. This finding suggests that the pes of animals, living in areas characterized by fluctuating water levels, and under conditions facilitating the preservation of footprints, were similar in form to those of extant semi‐aquatic avians.     

First evidence of the presence of chitin in skeletons of marine sponges. Part II. Glass sponges (Hexactinellida: Porifera)

Sponges (Porifera) are presently gaining increased scientific attention because of their secondary metabolites and specific skeleton structures. In contrast to demosponges, whose skeletons are formed from biopolymer spongin, glass sponges (hexactinellids) possess silica-organic composites as the main natural material for their skeletal fibres. Chitin has a crystalline structure and it constitutes a network of organized fibres. This structure confers rigidity and resistance to organisms that contain it, including monocellular (yeast, amoeba, diatoms) and multicellular (higher fungi, arthropods, nematodes, molluscs) organisms. In contrast to different marine invertebrates whose exoskeletons are built of chitin, this polysaccharide has not been found previously as an endogenous biopolymer within glass sponges (Hexactinellida). We hypothesized that glass sponges, which are considered to be the most basal lineage of multicellular animals, must possess chitin. Here, we present a detailed study of the structural and physico-chemical properties of skeletal fragments of the glass sponge Farrea occa. We show that these fibres have a layered design with specific compositional variations in the chitin/silica composite. We applied an effective approach for the demineralization of glass sponge skeletal formations based on an etching procedure using alkali solutions. The results show unambiguously that alpha-chitin is an essential component of the skeletal structures of Hexactinellida. This is the first report of a silica-chitin's composite biomaterial found in nature. From this perspective, the view that silica-chitin scaffolds may be key templates for skeleton formation also in ancestral unicellular organisms, rather than silica-protein composites, emerges as a viable alternative hypothesis.     

Estimating Mass Properties of Dinosaurs Using Laser Imaging and 3D Computer Modelling

Body mass reconstructions of extinct vertebrates are most robust when complete to near-complete skeletons allow the reconstruction of either physical or digital models. Digital models are most efficient in terms of time and cost, and provide the facility to infinitely modify model properties non-destructively, such that sensitivity analyses can be conducted to quantify the effect of the many unknown parameters involved in reconstructions of extinct animals. In this study we use laser scanning (LiDAR) and computer modelling methods to create a range of 3D mass models of five specimens of non-avian dinosaur; two near-complete specimens of Tyrannosaurus rex, the most complete specimens of Acrocanthosaurus atokensis and Strutiomimum sedens, and a near-complete skeleton of a sub-adult Edmontosaurus annectens. LiDAR scanning allows a full mounted skeleton to be imaged resulting in a detailed 3D model in which each bone retains its spatial position and articulation. This provides a high resolution skeletal framework around which the body cavity and internal organs such as lungs and air sacs can be reconstructed. This has allowed calculation of body segment masses, centres of mass and moments or inertia for each animal. However, any soft tissue reconstruction of an extinct taxon inevitably represents a best estimate model with an unknown level of accuracy. We have therefore conducted an extensive sensitivity analysis in which the volumes of body segments and respiratory organs were varied in an attempt to constrain the likely maximum plausible range of mass parameters for each animal. Our results provide wide ranges in actual mass and inertial values, emphasizing the high level of uncertainty inevitable in such reconstructions. However, our sensitivity analysis consistently places the centre of mass well below and in front of hip joint in each animal, regardless of the chosen combination of body and respiratory structure volumes. These results emphasize that future biomechanical assessments of extinct taxa should be preceded by a detailed investigation of the plausible range of mass properties, in which sensitivity analyses are used to identify a suite of possible values to be tested as inputs in analytical models.     

The origin of cellular life

This essay presents a scenario of the origin of life that is based on analysis of biological architecture and mechanical design at the microstructural level. My thesis is that the same architectural and energetic constraints that shape cells today also guided the evolution of the first cells and that the molecular scaffolds that support solid-phase biochemistry in modern cells represent living microfossils of past life forms. This concept emerged from the discovery that cells mechanically stabilize themselves using tensegrity architecture and that these same building rules guide hierarchical self-assembly at all size scales (Sci. Amer 278:48-57;1998). When combined with other fundamental design principles (e.g., energy minimization, topological constraints, structural hierarchies, autocatalytic sets, solid-state biochemistry), tensegrity provides a physical basis to explain how atomic and molecular elements progressively self-assembled to create hierarchical structures with increasingly complex functions, including living cells that can self-reproduce.     

Long-bone circumference and weight in mammals, birds and dinosaurs

The mid-shaft circumferences of the humerus and femur are closely related to body weight in living terrestrial vertebrates. Because these elements are frequently preserved in subfossil and fossil vertebrate skeletal materials, the relationship can be used to estimate body weight in extinct vertebrates. When the allometric equations are applied to the mid-shaft circumferences of these elements in dinosaurs, the weights calculated for some giant sauropods ( Brachiosaurus ) are found to be lighter than previous estimates.     

Calcite and aragonite distributions in the skeletons of bimineralic bryozoans as revealed by Raman spectroscopy

Abstract. Bryozoans are among a diverse range of invertebrates capable of secreting calcium carbonate skeletons. Relatively little is known about biomineralization in bryozoans, despite the importance of understanding biomineralization processes for nanotechnology and the threats imposed by ocean acidification on organisms having calcareous skeletons. Ten species of cheilostome bryozoans that are reported to have bimineralic skeletons of calcite and aragonite are studied here using Raman spectroscopy. This technique allowed identification of the two mineral phases at submicron spatial resolution, allowing the distributions of calcite and aragonite within bryozoan skeletons to be determined with unprecedented precision. Confirming previous findings based on the use of chemical stains, most of the bimineralic species analyzed exhibited a calcitic skeletal framework, composed of basal, vertical, and inner frontal walls, having aragonite deposited subsequently onto the outer surfaces of the frontal walls. In one species ( Odontionella cyclops ), aragonite formed the superstructure above the autozooids, and in two others, traces of aragonite were detected on the undersides of the frontal shields. Using Raman spectroscopy, it was possible for the first time to determine the mineralogy of small-scale structures, including orificial rims, condyles and hinge teeth, avicularian pivotal bars and rostra, and ascopore rims and sieve plates. Even when surrounded by aragonitic frontal shields, these structures were found typically to be calcitic, the two exceptions being the aragonitic avicularia of Stylopoma inchoans and O. cyclops . Unexpectedly, the first-formed part of the basal wall at the distalmost growing edge of Pentapora foliacea was found to consist mainly of aragonite. This may point to a precursory phase of biomineralization comparable with the unusual mineralogies identified previously in the earliest-formed skeletons of members of some other invertebrate phyla.     

Respiratory Evolution Facilitated the Origin of Pterosaur Flight and Aerial Gigantism

Pterosaurs, enigmatic extinct Mesozoic reptiles, were the first vertebrates to achieve true flapping flight. Various lines of evidence provide strong support for highly efficient wing design, control, and flight capabilities. However, little is known of the pulmonary system that powered flight in pterosaurs. We investigated the structure and function of the pterosaurian breathing apparatus through a broad scale comparative study of respiratory structure and function in living and extinct archosaurs, using computer-assisted tomographic (CT) scanning of pterosaur and bird skeletal remains, cineradiographic (X-ray film) studies of the skeletal breathing pump in extant birds and alligators, and study of skeletal structure in historic fossil specimens. In this report we present various lines of skeletal evidence that indicate that pterosaurs had a highly effective flow-through respiratory system, capable of sustaining powered flight, predating the appearance of an analogous breathing system in birds by approximately seventy million years. Convergent evolution of gigantism in several Cretaceous pterosaur lineages was made possible through body density reduction by expansion of the pulmonary air sac system throughout the trunk and the distal limb girdle skeleton, highlighting the importance of respiratory adaptations in pterosaur evolution, and the dramatic effect of the release of physical constraints on morphological diversification and evolutionary radiation.     

Overcoming the constraints of spiral growth: the case of shell remodelling

As animals grow in size, their relationship to the physical environment necessarily changes, but molluscs and brachiopods whose accretionary skeletons expand at one end of a hollow cone conform to logarithmic-spiral growth and retain a constant shape. Dissolution and remodelling of previously formed parts of the skeleton can alleviate the constraints of strict logarithmic-spiral growth. How, when, where and in which clades mineral skeletal resorption has evolved are important questions because they relate to the conditions and history of skeletal formation and to the way in which ocean acidification in the past influenced that history. A synthesis of data on mineral dissolution in shells shows that resorption from the inner surface of bivalve shells occurs under temporarily anaerobic conditions within the closed shell, but functional remodelling is unknown in bivalves. Resorption and functional remodelling occur in brachiopods, gastropods and terrestrial hermit crabs, and to a lesser extent in scaphopods and cephalopods. Internal whorl resorption leading to a more compact visceral mass has evolved at least ten times in gastropods. Contrary to expectations stemming from patterns in the availability of calcium, gastropod remodelling is a phenomenon of warm, calcium-rich environments and not of cold acidified conditions. There is therefore no evidence that internal whorl resorption increases calcium-use efficiency. Resorption is one of several mechanisms that have enabled animal skeletons to become more dynamic and adaptable during ontogeny.     

Relationship between osteology and aquatic locomotion in birds: determining modes of locomotion in extinct Ornithurae

The evolutionary history of aquatic invasion in birds would be incomplete without incorporation of extinct species. We show that aquatic affinities in fossil birds can be inferred by multivariate analysis of skeletal features and locomotion of 245 species of extant birds. Regularized discriminant analyses revealed that measurements of appendicular skeletons successfully separated diving birds from surface swimmers and flyers, while also discriminating among different underwater modes of swimming. The high accuracy of this method allows detection of skeletal characteristics that are indicative of aquatic locomotion and inference of such locomotion in bird species with insufficient behavioural information. Statistical predictions based on the analyses confirm qualitative assessments for both foot‐propelled (Hesperornithiformes) and wing‐propelled (Copepteryx) underwater locomotion in fossil birds. This is the first quantitative inference of underwater modes of swimming in fossil birds, enabling future studies of locomotion in extinct birds and evolutionary transitions among locomotor modes in avian lineage.     

In vivo molecular and cellular imaging with quantum dots

Quantum dots (QDs), tiny light-emitting particles on the nanometer scale, are emerging as a new class of fluorescent probe for in vivo biomolecular and cellular imaging. In comparison with organic dyes and fluorescent proteins, QDs have unique optical and electronic properties: size-tunable light emission, improved signal brightness, resistance against photobleaching, and simultaneous excitation of multiple fluorescence colors. Recent advances have led to the development of multifunctional nanoparticle probes that are very bright and stable under complex in vivo conditions. A new structural design involves encapsulating luminescent QDs with amphiphilic block copolymers and linking the polymer coating to tumor-targeting ligands and drug delivery functionalities. Polymer-encapsulated QDs are essentially nontoxic to cells and animals, but their long-term in vivo toxicity and degradation need more careful study. Bioconjugated QDs have raised new possibilities for ultrasensitive and multiplexed imaging of molecular targets in living cells, animal models and possibly in humans.     

The limits and frontiers of desiccation-tolerant life

Drying to equilibrium with the air is lethal to most speciesof animals and plants, making drought (i.e., low external waterpotential) a central problem for terrestrial life and a majorcause of agronomic failure and human famine. Surprisingly, awide taxonomic variety of animals, microbes, and plants do toleratecomplete desiccation, defined as water content below 0.1 g H₂Og^–1 dry mass. Species in five phyla of animals and fourdivisions of plants contain desiccation-tolerant adults, juveniles,seeds, or spores. There seem to be few inherent limits on desiccationtolerance, since tolerant organisms can survive extremely intenseand prolonged desiccation. There seems to be little phylogeneticlimitation of tolerance in plants but may be more in animals.Physical constraints may restrict tolerance of animals withoutrigid skeletons and to plants shorter than 3 m. Physiologicalconstraints on tolerance in plants may include control by hormoneswith multiple effects that could link tolerance to slow growth.Tolerance tends to be lower in organisms from wetter habitats,and there may be selection against tolerance when water availabilityis high. Our current knowledge of limits to tolerance suggeststhat they pose few obstacles to engineering tolerance in prokaryotesand in isolated cells and tissues, and there has already beenmuch success on this scientific frontier of desiccation tolerance.However, physical and physiological constraints and perhapsother limits may explain the lack of success in extending toleranceto whole, desiccation-sensitive, multicellular animals and plants.Deeper understanding of the limits to desiccation tolerancein living things may be needed to cross this next frontier.     

AIMS AND SCOPE

The Journal of Bionic Engineering publishes original research papers and reviews on all aspects of bionic science and engineering including fundamental understandings of animals and plants for bionic engineering, such as locomotion and behaviors of animals, structures, composites, morphology and physical properties of plants and natural materials, applications of such understandings in engineering, technology and designs.     

Taphonomy of coral reefs: a review

This review summarises the major factors that affect the post-mortem history of skeletons in a coral reef environment. Skeletal material is traced from life, through death, breakdown, transport, burial and diagenesis to its final fossil form. The fact that most reef sediments are of skeletal composition poses problems of concentration or dilution of individual grain types in taphonomic analysis of reefs. Rates of supply of grains vary, not only with organism abundance and skeletal growth rates, but also with rates of physical and biological breakdown to transportable sediment. Physical and organic processes affect sedimentary structures and textures by mixing or segregating skeletal grains, though biogenic processes normally dominate in the protected setting of reef lagoons. The soft and hard substrates associated with reefs present different media for calcium carbonate accumulation and post-depositional disturbance, for example, loose sediments suffer bioturbation and rocks surfaces suffer bioerosion. The wide range of durability of skeletons and their susceptibility to diagenesis contribute further to the complexities of the preservation of coral reefs.     

Ultrastructure and mineral distribution in the tergite cuticle of the beach isopod Tylos europaeus Arcangeli, 1938

The crustacean cuticle is a hierarchically organised material composed of an organic matrix and mineral. It is subdivided into skeletal elements whose physical properties are adapted to their function and the eco-physiological strains of the animal. Using a variety of ultrastructural and analytical techniques we studied the organisation of the tergite cuticle of the sand burrowing beach isopod Tylos europaeus. The surface of the tergites bear epicuticular scales, sensilla and micro-tubercles. A distal layer of the exocuticle is characterised by a low density of organic fibres and the presence of magnesium-calcite. Surprisingly, the mineral forms regions containing polyhedral structures alternating with smooth areas. Between sub-domains within the distal exocuticle calcite varies in its crystallographic orientation. Proximal layers of the exocuticle and the endocuticle are devoid of calcite and the mineral occurs in the form of amorphous calcium carbonate (ACC). Using thin sections of mineralised cuticle we describe for the first time that ACC forms tubes around single protein-chitin fibrils.     

Requirements for comparing the performance of finite element models of biological structures

The widespread availability of three-dimensional imaging and computational power has fostered a rapid increase in the number of biologists using finite element analysis (FEA) to investigate the mechanical function of living and extinct organisms. The inevitable rise of studies that compare finite element models brings to the fore two critical questions about how such comparative analyses can and should be conducted: (1) what metrics are appropriate for assessing the performance of biological structures using finite element modeling? and, (2) how can performance be compared such that the effects of size and shape are disentangled? With respect to performance, we argue that energy efficiency is a reasonable optimality criterion for biological structures and we show that the total strain energy (a measure of work expended deforming a structure) is a robust metric for comparing the mechanical efficiency of structures modeled with finite elements. Results of finite element analyses can be interpreted with confidence when model input parameters (muscle forces, detailed material properties) and/or output parameters (reaction forces, strains) are well-documented by studies of living animals. However, many researchers wish to compare species for which these input and validation data are difficult or impossible to acquire. In these cases, researchers can still compare the performance of structures that differ in shape if variation in size is controlled. We offer a theoretical framework and empirical data demonstrating that scaling finite element models to equal force: surface area ratios removes the effects of model size and provides a comparison of stress-strength performance based solely on shape. Further, models scaled to have equal applied force:volume ratios provide the basis for strain energy comparison. Thus, although finite element analyses of biological structures should be validated experimentally whenever possible, this study demonstrates that the relative performance of un-validated models can be compared so long as they are scaled properly.