Jorge Cubo

Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs.

The first quantitative experimental data on growth dynamics of the primary cortical bone of young ratites demonstrate the following. 1) From hatching to 2 months of age, cortical thickness remains constant, thereby expressing equilibrium between periosteal bone deposition and an endosteal bone resorption. 2) Radial growth rates of the diaphyseal bone cortex are high (10-40 microns.day-1 on average--maximum 80 microns.day-1) in the hindlimb (femur, tibiotarsus and tarsometatarsus). Wing bones are smaller and later developed. They have lower rates of radial osteogenesis (2-14 microns.day-1). 3) High growth rates are linked to densely vascularized primary bone belonging to the reticular or laminar tissue types. Growth rates fall when bone vascular density decreases. These results emphasize the importance of examining a large number of skeletal elements in order to build a precise knowledge of the general relationship between bone growth rate and bone tissue type. They also stress the potential of bone growth rate quantification among extinct tetrapods, including non-avian dinosaurs.

Phylogenetic Signal in Bone Microstructure of Sauropsids

In spite of the fact that the potential usefulness of bone histology in systematics has been discussed for over one and a half centuries, the presence of a phylogenetic signal in the variation of histological characters has rarely been assessed. A quantitative assessment of phylogenetic signal in bone histological characters could provide a justification for performing optimizations of these traits onto independently generated phylogenetic trees (as has been done in recent years). Here we present an investigation on the quantification of the phylogenetic signal in the following bone histological, microanatomical, and morphological traits in a sample of femora of 35 species of sauropsids: vascular density, vascular orientation, index of Haversian remodeling, cortical thickness, and cross-sectional area (bone size). For this purpose, we use two methods, regressions on distance matrices tested for significance using permutations (a Mantel test) and random tree length distribution. Within sauropsids, these bone microstructural traits have an optimal systematic value in archosaurs. In this taxon, a Mantel test shows that the phylogeny explains 81.8% of the variation of bone size and 86.2% of the variation of cortical thickness. In contrast, a Mantel test suggests that the phylogenetic signal in histological traits is weak: although the phylogeny explains 18.7% of the variation of vascular density in archosaurs, the phylogenetic signal is not significant either for vascular orientation or for the index of Haversian remodeling. However, Mantel tests seem to underestimate the proportion of variance of the dependent character explained by the phylogeny, as suggested by a PVR (phylogenetic eigenvector) analysis. We also deal with some complementary questions. First, we evaluate the functional dependence of bone vascular density on bone size by using phylogenetically independent contrasts. Second, we perform a variation partitioning analysis and show that the phylogenetic signal in bone vascular density is not a by-product of phylogentic signal in bone size. Finally, we analyze the evolution of cortical thickness in diapsids by using an optimization by squared change parsimony and discuss the functional significance of this character in terms of decreased buoyancy in crocodiles and mass saving in birds. These results are placed in the framework of the constructional morphology model, according to which the variation of a character in a clade has a historical (phylogenetic) component, a functional (adaptive) component, and a structural (architectural) component.

Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes

SUMMARY The biological features observed in every living organism are the outcome of three sets of factors: historical (inherited by homology), functional (biological adaptation), and structural (properties inherent to the materials with which organs are constructed, and the morphogenetic rules by which they grow). Integrating them should bring satisfactory causal explanations of empirical data. However, little progress has been accomplished in practice toward this goal, because a methodologically efficient tool was lacking. Here we use a new statistical method of variation partitioning to analyze bone growth in amniotes. (1) Historical component. The variation of bone growth rates contains a significant phylogenetic signal, suggesting that the observed patterns are partly the outcome of shared ancestry. (2) Functional causation. High growth rates, although energy costly, may be adaptive (i.e., they may increase survival rates) in taxa showing short growth periods (e.g., birds). In ectothermic amniotes, low resting metabolic rates may limit the maximum possible growth rates. (3) Structural constraint. Whereas soft tissues grow through a multiplicative process, growth of mineralized tissues is accretionary (additive, i.e., mineralization fronts occur only at free surfaces). Bone growth of many amniotes partially circumvents this constraint: it is achieved not only at the external surface of the bone shaft, but also within cavities included in the bone cortex as it grows centrifugally. Our approach contributes to the unification of historicism, functionalism, and structuralism toward a more integrated evolutionary biology.

Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus

Abstract In primates, age determination using lines of arrested growth (LAGs) from bones has rarely been attempted, andthe reliability of these structures has never been experimentally validated. In order to test skeletochronology inprimates, LAGs were studied mainly in the long bones of known age Microcebus murinus , a small primate, whosepotential longevity may reach 12 years. LAGs were extensively studied in 43 males and 23 females ranging fromjuveniles to 11-year-old adults. All individuals were born and reared in captivity. Some young individuals wereinjected with fluorescent dyes to quantify bone growth rates. LAGs in the diaphysis of the tibia are well correlatedwith age and this skeletal element appears to be the best for assessing skeletochronology in Microcebus murinus .There is strong evidence that the seasonal cycle of photoperiodicity is more important than age alone in producingLAGs. Key words : age determination, skeletochronology, primates, Microcebus murinus INTRODUCTION

The Gavialis--Tomistoma debate: the contribution of skull ontogenetic allometry and growth trajectories to the study of crocodylian relationships

SUMMARY The phylogenetic placement of Tomistoma and Gavialis crocodiles depends largely upon whether molecular or morphological data are utilized. Molecular analyses consider them as sister taxa, whereas morphological/paleontological analyses set Gavialis apart from Tomistoma and other crocodylian species. Here skull allometric trajectories of Tomistoma and Gavialis were contrasted with those of two longirostral crocodylian taxa, Crocodylus acutus and Mecistops cataphractus, to examine similarities in growth trajectories in light of this phylogenetic controversy. Entire skull shape and its two main modules, rostrum and postrostrum, were analyzed separately. We tested differences for both multivariate angles between trajectories and for shape differences at early and late stages of development. Based on a multivariate regression of shape data and size, Tomistoma seems to possess a peculiar rate of growth in comparison to the remaining taxa. However, its morphology at both juvenile and adult sizes is always closer to those of Brevirostres crocodylians, for the entire head shape, as well as the shape of the postrostrum and rostrum. By contrast, the allometric trajectory of Gavialis always begins and ends in a unique region of the multidimensional morphospace. These findings concur with a morphological hypothesis that places Gavialis separate from Brevirostres, and Tomistoma closer to other crocodylids, and provides an additional, and independent, data set to inform on this ongoing phylogenetic discussion.

Paleohistological estimation of bone growth rate in extinct archosaurs

Abstract The clade Archosauria contains two very different sister groups in terms of diversity (number of species) and disparity (phenotypic variation): Crurotarsi (taxa more closely related to crocodiles than to birds) and Ornithodira (pterosaurs and dinosaurs including birds). The extant species of Crurotarsi may constitute a biased sample of past biodiversity regarding growth patterns and metabolic rates. Bone histological characters can be conserved over hundreds of millions of years in the fossil record and potentially contain information about individual age at death, age at sexual maturity, bone growth rates, and basal metabolic rates of extinct vertebrates. Using a sample of extant amniotes, we have constructed a paleobiological model to estimate bone growth rate from bone histological traits. Cross-validation tests show that this model is reliable. We then used it to estimate bone growth rates in a sample of extinct archosaurs including Crurotarsi and Ornithodira. After testing for phylogenetic signal, optimization of femoral growth rates through squared change parsimony onto a time-calibrated tree of amniotes shows two divergent evolutionary trends: whereas bone growth rates increase from the last common ancestor of Ornithodira to extant birds, they decrease from the last common ancestor of Crurotarsi to extant crocodiles. However, we conclude, on the basis of recent evidence for unidirectional airflow in the lungs of alligators, that crocodiles may have retained the capacity of growing at high rates.

Variation of the Outer Circumferential Layer in the Limb Bones of Birds

Abstract. The core of the limb bone cortex of mammals and birds is made of rapidly deposited, fibro-lamellar bone tissue (also present in non-avian theropods), which is usually surrounded by an avascular outer circumferential layer (OCL) of slowly deposited parallel-fibered bone. We present the first comparative allometric study of the relative OCL thickness (expressed as a fraction of the diaphyseal radius) in modern birds. Body size explains 79% of the OCL variation in thickness, which is inversely correlated with size, that is, shows negative allometry (slope -0.799). This may explain the apparent absence of OCL in the ratites. Since the OCL is deposited at the end of growth, we propose that its relative thickness probably correlates with the amount of slow, residual growth, which our results suggest to be on the average larger in small birds.

Bone growth marks reveal protracted growth in New Zealand kiwi (Aves, Apterygidae)

The presence of bone growth marks reflecting annual rhythms in the cortical bone of non-avian tetrapods is now established as a general phenomenon. In contrast, ornithurines (the theropod group including modern birds and their closest relatives) usually grow rapidly in less than a year, such that no annual rhythms are expressed in bone cortices, except scarce growth marks restricted to the outer cortical layer. So far, cyclical growth in modern birds has been restricted to the Eocene Diatryma, the extant parrot Amazona amazonica and the extinct New Zealand (NZ) moa (Dinornithidae). Here we show the presence of lines of arrested growth in the long bones of the living NZ kiwi (Apteryx spp., Apterygidae). Kiwis take 5–6 years to reach full adult body size, which indicates a delayed maturity and a slow reproductive cycle. Protracted growth probably evolved convergently in moa and kiwi sometime since the Middle Miocene, owing to the severe climatic cooling in the southwest Pacific and the absence of mammalian predators.

Evidence for High Bone Growth Rate in Euparkeria Obtained Using a New Paleohistological Inference Model for the Humerus

ABSTRACT The study of bone growth rate and metabolic rate evolution in archosaurs (crocodiles, dinosaurs including birds, and pterosaurs) and close outgroups has become a subject of major interest among paleontologists in recent years. In this paper, we estimate the bone growth rate of Euparkeria using a new statistical inference model for the humerus. We modified the taxonomic range of extant species used in previous studies, on which we performed quantitative measurements of histological features and bone growth rates. Bone growth rate values estimated for Euparkeria are crucial in understanding the ancestral condition for archosaurs because this taxon is considered the closest relative to the archosaur crown group. We obtained an instantaneous growth rate of 6.12 µm/day, suggesting that Euparkeria shared with other non-archosaurian archosauromorphs (Prolacerta, Proterosuchus, and Erythrosuchus) a condition of high growth rate compatible with endothermy. This derived state may have been inherited by some Triassic crurotarsans, as suggested by the high instantaneous bone growth rate (14.52 µm/day) estimated in this study for Postosuchus. Jurassic crurotarsans may have lost endothermy during the transition from terrestrial habitats and active predation to aquatic habitats and sit-and-wait predation behaviors, so that Cretaceous crocodiles may be secondarily ectothermic, as suggested by &dgr;18O values. In conclusion, we provide new evidence for the hypothesis of an ancestral endothermic state for the last common ancestor of archosaurs, and show that non-archosaurian archosauromorphs and Triassic crurotarsans may have been characterized by a thermometabolism more similar to that of dinosaurs than to that of lepidosaurs and turtles.

Pattern and process in constructional morphology.

In Chapter 10 of the masterful book The Structure of Evolutionary Theory, Gould (2002) expands a model first proposed by Seilacher (1970) that explains the genesis of adaptive morphological features of organisms as the outcome of the action of three causal factors that form a triangle in a theoretical space. These factors are phylogenetic (Historischphylogenetischer Aspekt), adaptational (Ökologisch-adaptiver Aspekt), and architectural (Bautechnischer Aspekt) for Seilacher (1970) and historical, functional, and structural for Gould (2002, p. 1052). The position of any morphological character within the surface of the triangle is determined by the relative contribution of each one of these causal factors to explain the variation of this character. For instance, morphological stasis can be mainly determined by limited genetic variation (a historical factor), stabilizing selection (a functional factor), or be imposed by a physical law (a structural factor). This framework is known as constructional morphology (McGhee 1999). Recent findings in evo-devo show that different phyla share homologous genes and similar developmental mechanisms (‘‘deep homology,’’ for instance, the existence of Hox genes regulating the differentiation of regions along the anterior–posterior axis in Arthropods and Vertebrates; Gilbert 2000, p. 366). This evidence, together with new insights into the role of self-organization in development (Seilacher 1991; Kauffman 1993), suggest that historical and structural factors are more important than traditionally assumed by Neo-Darwinism. In this context, Seilacher’s model is of high interest and deserves wider recognition not only because of its high heuristic value, but also because it integrates three main world views in biology that, following Gould (2002, pp. 1057–1061), are historicism (genealogical cladism), Darwinian functionalism (the adaptational paradigm), and physical structuralism (D’Arcy Thompsonism and spandrelism; see below). Here I address the question of whether historical and structural factors are mechanisms different from the functional mechanism of natural selection as causes of adaptive evolutionary change.