Inferring the physiological regimes of extinct vertebrates: methods, limits and framework.

What can we know of the physiological regimes of ancient vertebrates? Essential to the exploration of this question are several epistemological tools: (i) a phylogenetic framework for interpreting whole animals and individual tissues, (ii) reliable knowledge of variation in populations and among climates and geographies, (iii) an understanding of phenotypic variation during ontogeny and between sexes, and (iv) a sense of the patterns of body size change, both phyletically and ontogenetically. Palaeobiologists are historically bound to a dichotomous set of terms developed long ago to describe the relatively depauperate living vertebrate fauna. This system sees only binary categories of five major groupings: the 'cold-blooded' fishes, amphibians, and reptiles, and the 'warm-blooded' birds and mammals. The integration of histoanatomical data with patterns of size, growth and phylogeny provides an opportunity to re-imagine not only vertebrate palaeophysiology, but vertebrate physiology in general. Here, we discuss how four 'signals' or 'influences' on bone tissues-phylogeny, ontogeny, mechanics and environment-can help to address these questions. This article is part of the theme issue 'Vertebrate palaeophysiology'.

Globuli ossei in the long limb bones of Pleurodeles waltl (Amphibia, Urodela, Salamandridae).

To date, little is known about the structure of the cells and the fibrillar matrix of the globuli ossei, globular structures showing histochemical properties of an osseous tissue, sometimes found in the resorption front of the hypertrophied cartilage in many tetrapods, and easily observed in the long bones of the Urodele Pleurodeles waltl. Here, we present the results obtained from the appendicular long bones of metamorphosed juveniles and subadults using histological and histochemical methods and transmission electron microscopy. The distal part of the cone-shaped cartilage contains a heterogeneous cell population composed of the typical "light" hypertrophic chondrocytes and scarce "dark" hypertrophic chondrocytes. The "dark" chondrocytes display ultrastructural characteristics suggesting that they probably undergo degeneration through chondroptosis. However, in the hypertrophic, calcified cartilage close to the erosion front by the marrow, several noninvaded chondrocytic lacunae retained cells that do not show any morphological characteristics of degeneration and that cannot be identified as regular chondrocytes or osteocytes. These modified chondrocytes that have lost their regular morphology, appear to be active in the terminal cartilage and synthesize collagen fibrils of a peculiar diameter intermediate between the Type I collagen found in bone and the Type II collagen characteristic of cartilage. It is suggested that the local occurrence of globuli ossei is linked to a low rate of longitudinal growth as is the case in the long bones of postmetamorphic urodeles.

Developmental plasticity of limb bone microstructural organization in Apateon: histological evidence of paedomorphic conditions in branchiosaurs.

Apateon, a key genus among Branchiosauridae from the Carboniferous--Permian of Europe, is often considered closely related to salamanders on the basis of developmental similarities, anatomical features, and life history. The current work deals with recognition of heterochronies among three "time-averaged populations" of Apateon based on inference from histological features already studied in extant urodeles. Our study is performed on the long bones of 22 specimens of Apateon pedestris and Apateon caducus. Histological observations show that diaphyseal and epiphyseal ossification patterns of Apateon are similar to those of urodeles. From skeletochronological analysis, the identification of the age of sexual maturity allows us to discriminate juveniles from adults and to confirm the previous hypothesis of a paedomorphic condition based on anatomical data among these species. The current study also suggests a paedomorphic condition of each "population" at the histological level. This heterochrony may have been linked to peculiar ecological conditions such as hypoxic and fresh water environment. Functional reasons may also be invoked to explain differences of ossification between fore- and hindlimbs of the "populations" from Odernheim and Niederkirchen because paleoecological conditions are very different from one locality to another. This study illustrates the role that the acquisition of heterochronic features plays at the microevolutionary scale.

On Darwin's palaeontology in The origin of species.

I investigate the role of palaeontology within Darwin's works through an analysis of the two chapters of The Origin of Species most especially devoted to this science. Palaeontology may occupy several places within the structure of the argumentative logic of Darwinism, but these places have remained to some extent ancillary. Indeed, palaeontology could well document evolutionary patterns, showing the actual occurrence of evolution as a general "historical fact", but it was poorly adapted to demonstrate the main point of Darwinism: the actual evolutionary process: natural selection acting among individuals. I also show, in agreement with Gould, that Darwin had great confidence in the ultimate ability of palaeontology to support his theory, and that in interpreting palaeontological evidence, he expressed a vision of natural selection much wider and more eclectic than that which has generally been ascribed to him.

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.

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

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.