Ontogeny of the syndesmosis tibiofibularis and the evolution of the bird hindlimb: a caenogenetic feature triggers phenotypic novelty

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Abstract
The underlying theme of this study is the contribution of developmental mechanisms to the generation of morphological novelty in evolution. The syndesmosis tibiofibularis, an important structural and functional link between the two zeugopod bones of the bird hindlimb, is used as a model for evolutionary novelty. We analyze the structural, developmental and adaptive aspects of its origin in a combined descriptive, experimental, and comparative approach.The ontogeny of the syndesmosis in the chick embryo involves several developmental steps, including the formation of a separate cartilage rudiment that in turn stimulates the formation of an osseous crest on the tibia, which with eventually replace the cartilage element itself. Some of the epigenetic requirements for the formation of the cartilage element and the osseous crest are demonstrated by experimentally increasing the distance between the two zeugopod bones, an operation that results in the absence of both cartilage and crest. Although a syndesmosis tibiofibularis associated with an osseous crest on the tibiotarsus is unique to birds in extant vertebrates, the presence of a distinct crest at the corresponding location in theropod dinosaurs indicates that a syndesmosis also existed in this group of archosaurs.The results of the study suggest that in the case of the syndesmosis tibiofibularis phenotypic evolutionary novelty is based on a caenogenetic feature, i.e. a feature that initially arose in response to changing developmental conditions. In conclusion we propose a model for the stepwise evolutionary modification of the sauropsid hindlimb, integrating adaptive trends and developmental mechanisms that interactively determine the transformations of skeletal limb morphology. The syndesmosis tibiofibularis and the mechanisms of its formation are not only shown to have played a key-role in this process, but its presence in theropod dinosaurs also points towards the origin of birds.