Abstract
Performance of the masticatory system directly influences feeding and survival, so adaptive hypotheses often are proposed to explain craniodental evolution via functional morphology changes. However, the prevalence of “many-to-one” association of cranial forms and functions in vertebrates suggests a complex interplay of ecological and evolutionary histories, resulting in redundant morphology-diet linkages. Here we examine the link between cranial biomechanical properties for taxa with different dietary preferences in crown clade Carnivora, the most diverse clade of carnivorous mammals. We test whether hypercarnivores and generalists can be distinguished based on cranial mechanical simulation models, and how such diet-biomechanics linkages relate to morphology. Comparative finite element and geometric morphometrics analyses document that predicted bite force is positively allometric relative to skull strain energy; this is achieved in part by increased stiffness in larger skull models and shape changes that resist deformation and displacement. Size-standardized strain energy levels do not reflect feeding preferences; instead, caniform models have higher strain energy than feliform models. This caniform-feliform split is reinforced by a sensitivity analysis using published models for six additional taxa. Nevertheless, combined bite force-strain energy curves distinguish hypercarnivorous versus generalist feeders. These findings indicate that the link between cranial biomechanical properties and carnivoran feeding preference can be clearly defined and characterized, despite phylogenetic and allometric effects. Application of this diet-biomechanics linkage model to an analysis of an extinct stem carnivoramorphan and an outgroup creodont species provides biomechanical evidence for the evolution of taxa into distinct hypercarnivorous and generalist feeding styles prior to the appearance of crown carnivoran clades with similar feeding preferences.
Highlights
Measures of biological function and performance link morphological variation with survival and reproductive fitness, and are a means of identifying functional morphological adaptations [1]
We investigate form-function mapping through a combination of shape analysis using geometric morphometrics (GMM) and biomechanical simulations, with a modeling approach based on Finite Element Analysis (FEA)
Results of FE analyses show an isometric relationship between input load and output bite force (Fig 2A and Table 2); this trend is significant in both regression analyses of the raw values and phylogenetic independent contrasts (PICs)
Summary
Measures of biological function and performance link morphological variation with survival and reproductive fitness, and are a means of identifying functional morphological adaptations [1]. The nearly complete reliance on analysis of morphological characteristics that are amenable to fossilization introduces difficulties in establishing a morphology-diet linkage model between predicted functional morphology and known feeding preferences of extant species. Interpretations of the paleobiology of extinct species and their evolutionary trends may be confounded by the ubiquitous phenomenon of many-to-one form-function mapping in vertebrate structures [2]. One biological function may be performed by morphologies taking many forms, and vice versa. Developing methods for successfully deciphering the relationships between form and function in spite of this complexity, is critical for enhancing our understanding of morphological adaptations, both in living ecological webs and through deep time, as well as how the patterns of functional innovations co-varied with diversification and extinction patterns
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