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.