Functional Evolution and Modular Behaviour in the Carnivoran Mandible

Abstract

Synopsis The relationship between form and function holds a central spot in evolutionary biology, as the changes in such relationship through time, are likely to deeply influence how organisms adapt to the surrounding environment. However, anatomical structures may be interpreted as a compound of so-called “modules” which may respond differently to similar biomechanical demands. To understand the extent of how the form of a modular structure relate to biomechanical performance, we combined modern 3D shape analysis with phylogenetic comparative methods, to determine whether evolutionary rates of shape are correlated with evolutionary rates of different functions. Here, we quantified the shape of 91 mandibles belonging to 67 species of eutherian carnivores and used three distinct performance metrics such as canine bite force, mechanical advantage of temporalis and masseter muscles. Results showed a large decoupling of evolutionary rates of shape and function, suggesting that many-to-one mapping of form and function plays a relevant role in obscuring a direct relationship between form and function rates of evolution. However, when we performed a robust phylogenetic regression, we found a significant relationship between evolutionary rates of mandibular shape and the mechanical advantage of the temporalis muscle. This suggests that the evolution of the mandible may show a modular behavior, hinting that different regions of the same structure may evolve at different paces and hence display different degree of correlation. In conclusion, our results highlight that even simpler anatomical structures are likely to display a mosaic evolution rather showing a direct, one-to-one, relationship between form and function.