Relationship between bone growth rate and bone tissue organization in amniotes: first test of Amprino's rule in a phylogenetic context

A debate on the determinism (phylogenetic versus functional) of the diversity of bone histological features has centred the interest of bone comparative biologists. While some authors have noticed the presence of a phylogenetic signal in bone tissue variation, many others have argued that these characters may not include much phylogenetic information, but rather reflect functional factors. Here we quantify both components in a sample of amniotes. We hypothesize that: 1/ the observed variation is partly the outcome of shared ancestry (phylogenetic factor) and 2/ for a given quantity of bone produced, tissues formed at a rapid rate may have a higher fraction of vascular cavities than those produced at a slower rate (functional factor). Variation partitioning analyses show that the phylogeny explains a significant portion of the variation of bone vascularity (85.3%), bone growth rate also explains a significant portion of this variation (68.3%), and there is an important overlap (67.9%). Finally, an optimization through least-squares parsimony of bone growth rates onto the phylogeny shows that the most important evolutionary change may have occurred after the split between crocodiles and birds. This change may be linked to the origin of avian endothermic metabolism because high growth rates involve high protein turnover, which is very energy consuming. We conclude that the debate on the dichotomy between phylogenetic versus functional causation of bone histological diversity is misleading, because we have shown that bone vascularity has, at the same time, a functional significance and a phylogenetic signal. (C) Koninklijke Brill NV, Leiden, 2010.