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Microstructure-function relationships remain poorly understood in primary bone tissues. The relationship between bone growth rate and bone tissue type, although documented in some species by previous works, remains somewhat unclear and controversial. We assessed this relationship in a species with extreme adaptations, the king penguin (Aptenodytes patagonicus). These birds have a peculiar growth, interrupted 3·months after hatching by the austral winter. Before this interruption, chicks undergo extremely rapid statural and ponderal growth. We recorded experimentally (by means of fluorescent labelling) the growth rate of bone tissue in four long bones (humerus, radius, femur and tibiotarsus) of four king penguin chicks during their fastest phase of growth (3-5·weeks after hatching) and identified the associated bone tissue types ('laminar', 'longitudinal', 'reticular' or 'radial' fibro-lamellar bone tissue). We found the highest bone tissue growth rate known to date, up to 171·µm·day -1 (mean 55·µm·day -1 ). There was a highly significant relationship between bone tissue type and growth rate (P<10 -6 ). Highest rates were obtained with the radial microarchitecture of fibro-lamellar bone, where cavities in the woven network are aligned radially. This result supports the heuristic value of a relationship between growth rate and bone primary microstructure. However, we also found that growth rates of bone tissue types vary according to the long bone considered (P<10 -5 ) (e.g. growth rates were 38% lower in the radius than in the other long bones), a result that puts some restriction on the applicability of absolute growth rate values (e.g. to fossil species). The biomechanical disadvantages of accelerated bone growth are discussed in relation to the locomotor behaviour of the chicks during their first month of life.

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Here we study the occurrence of torsion-resisting morphological and histological features (thin bone walls, circular shaft cross-section, oblique collagen fibers, and laminar tissue arrangement) in a sample of 168 long bones from wings and legs of 22 bird species. These structural parameters were measured in mid diaphyseal undemineralized cross-sections and analyzed using uni-, bi-, and multivariate (principal components analysis) data analysis techniques. We found that the four variables are significantly and positively correlated, and that covariation between variables accounts for as much as 58% of the total variation. These results suggest that torsion is a main determinant of the macro-and microstructural design of long bones in birds. Humerus, ulna, and femur generally possess torsion-resisting features, while other bones (radius, carpometacarpus, tibiotarsus, tarsometatarsus, and foot phalanx) rather show bending/axial load-resisting structural properties. These results are congruent with in vivo strain data from the literature, which reported high torsional loading in humerus and ulna during flapping flight, but also in the subhorizontal avian femur during terrestrial locomotion. The precise function of the laminar tissue spatial arrangement, the role of pneumatization, and the influence of flight mode are discussed.

In primates, age determination using lines of arrested growth (LAGs) from bones has rarely been attempted, and the reliability of these structures has never been experimentally validated. In order to test skeletochronology in primates, LAGs were studied mainly in the long bones of known age Microcebus murinus, a small primate, whose potential longevity may reach 12 years. LAGs were extensively studied in 43 males and 23 females ranging from juveniles to 11-year-old adults. All individuals were born and reared in captivity. Some young individuals were injected with fluorescent dyes to quantify bone growth rates. LAGs in the diaphysis of the tibia are well correlated with 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 producing LAGs.

Summary 1.Integrative studies on ageing patterns in multiple traits of organisms are challenging and rare in free-living populations. However, developing integrative approaches could prove useful to understanding ageing patterns as causes of age variations are diverse, with conflicting or related actions. Accordingly, we investigated age variation of multiple aspects in the common lizard Lacerta (Zootoca) vivipara. 2. In a wild population of common lizards, we studied five fitness components, three physiological traits (cell-mediated immunity, corticosterone level, resting metabolic rate), and controlled for individual and environmental heterogeneities. To quantify ageing patterns in fitness, we used individual-based data collected over 14 years (18 684 captures, 892 reproductive events). 3. Ageing patterns were found in multiple aspects. They provided evidence for female maturation early in adulthood (access to reproduction, litter size), followed by senescence in female reproduction (litter success) and survival. In parallel to senescence, a pattern of terminal investment enhanced offspring quality (offspring body size, offspring corpulence, litter success). Ageing patterns involved physiology with higher metabolic rate and T cell-mediated immune response in old females. 4. Several ageing patterns were dependent on environmental and individual characteristics (habitat, year, sex, body size). Interestingly, senescence occurred only in females with a high reproductive effort early in life. Rarely showed, this trade-off between early and late-life performances is expected under the antagonistic pleiotropy and disposable soma theories of senescence. 5. Overall, this study emphasizes the interest of integrative studies to investigate the multifaceted process of ageing.

Metabolic heat production in archosaurs has played an important role in their evolutionary radiation during the Mesozoic, and their ancestral metabolic condition has long been a matter of debate in systematics and palaeontology. The study of fossil bone histology provides crucial information on bone growth rate, which has been used to indirectly investigate the evolution of thermometabolism in archosaurs. However, no quantitative estimation of metabolic rate has ever been performed on fossils using bone histological features. Moreover, to date, no inference model has included phylogenetic information in the form of predictive variables. Here we performed statistical predictive modeling using the new method of phylogenetic eigenvector maps on a set of bone histological features for a sample of extant and extinct vertebrates, to estimate metabolic rates of fossil archosauromorphs. This modeling procedure serves as a case study for eigenvector-based predictive modeling in a phylogenetic context, as well as an investigation of the poorly known evolutionary patterns of metabolic rate in archosaurs. Our results show that Mesozoic theropod dinosaurs exhibit metabolic rates very close to those found in modern birds, that archosaurs share a higher ancestral metabolic rate than that of extant ectotherms, and that this derived high metabolic rate was acquired at a much more inclusive level of the phylogenetic tree, among non-archosaurian archosauromorphs. These results also highlight the difficulties of assigning a given heat production strategy (i.e., endothermy, ectothermy) to an estimated metabolic rate value, and confirm findings of previous studies that the definition of the endotherm/ectotherm dichotomy may be ambiguous.

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.