How ecological opportunity relates to diversification is a central question in evolutionary biology. However, there are few empirical examples of how ecological opportunity and morphological innovation open new adaptive zones, and promote diversification. We analyse data on diet, skull morphology and bite performance, and relate these traits to diversification rates throughout the evolutionary history of an ecologically diverse family of mammals (Chiroptera: Phyllostomidae). We found a significant increase in diversification rate driven by increased speciation at the most recent common ancestor of the predominantly frugivorous subfamily Stenodermatinae. The evolution of diet was associated with skull morphology, and morphology was tightly coupled with biting performance, linking phenotype to new niches through performance. Following the increase in speciation rate, the rate of morphological evolution slowed, while the rate of evolution in diet increased. This pattern suggests that morphology stabilized, and niches within the new adaptive zone of frugivory were filled rapidly, after the evolution of a new cranial phenotype that resulted in a certain level of mechanical efficiency. The tree-wide speciation rate increased non linearly with a more frugivorous diet, and was highest at measures of skull morphology associated with morphological extremes, including the most derived Stenodermatines. These results show that a novel stenodermatine skull phenotype played a central role in the evolution of frugivory and increasing speciation within phyllostomids.
The wide range of dietary niches filled by modern mammals is reflected in morphological diversity of the feeding apparatus. Despite volumes of data on the biomechanics of feeding, the extent to which the shape of mammal skulls reflects stresses generated by feeding is still unknown. In addition to the feeding apparatus, the skull accommodates the structural needs of the sensory systems and brain. We turned to bats as a model system for separating optimization for masticatory loads from optimization for other functions. Because the energetic cost of flight increases with body mass, it is reasonable to suggest that bats have experienced selective pressure over evolutionary time to minimize mass. Therefore, the skulls of bats are likely to be optimized to meet functional demands. We investigate the hypothesis that there is a biomechanical link between biting style and craniofacial morphology by combining biting behavior and bite force data gathered in the field with finite-element (FE) analysis. Our FE experiments compared patterns of stress in the craniofacial skeletons within and between two species of bats (Artibeus jamaicensis and Cynopterus brachyotis) under routine and atypical loading conditions. For both species, routine loading produced low stresses in most of the skull. However, the skull of Artibeus was most resistant to loads applied via its typical biting style, suggesting a mechanical link between routine loading and skull form. The same was not true of Cynopterus, where factors other than feeding appear to have had a more significant impact on craniofacial morphology. Key words: biting behavior; bone stress; adaptation; finite-element analysis; Chiroptera Mammal evolution is largely a story of the expansion of dietary niches from an insect-eating ancestor to include foods ranging from meat and bone to plankton. This diversity is clearly reflected in the morphology of the craniofacial skeleton. The association between skull structure and diet across distantly related mammals suggests that skull shape underwent selection over evolutionary time as new dietary niches were explored. Many excellent laboratory-based studies of feeding have provided a wealth of detailed information about the biomechanical behavior of bones and muscles under controlled experimental conditions. Building on this knowledge, morphologists are beginning to venture into the field to investigate how natural behaviors interact with morphology to define how animals function within their native environments. By
Summary1. In vertebrates, bite force is a measure of whole organism performance that is associated with both cranial morphology and dietary ecology. Mechanistic studies of bite force production have identified morphological features associated with bite force, and linked bite force with diet, but this approach has rarely been used in mammals. 2. Mammals are a good system with which to investigate the function of the feeding apparatus because of the relative simplicity of their skulls and their high dietary diversity. Phyllostomid bats are one of the most trophically and morphologically diverse groups of mammals, but we know little about the relative importance of biomechanical variables in producing bite force or how these variables vary with diet. 3. We combined in vivo measurements of bite force with assessments of muscular and bony morphology to build and validate a model describing the mechanics of bite force production in 25 species of bats. We used this model to investigate how bats with different diets vary in biomechanical parameters that contribute to bite force. In addition to traditional dietary categories, we used a functional definition of diet that reflects the mechanical demands (hardness) of the food items in the natural diet. 4. Our model provided good predictions of in vivo bite forces and highlighted behavioural variation that is inherent in the in vivo data. The temporalis generates the highest moment about the temporomandibular joint (TMJ) axis, but the moment generated by the masseter is the most important variable in explaining variation among species. The dietary classification based on the hardness of the diet was more effective than traditional dietary categories in describing biomechanical differences among groups. The temporalis generated the highest proportion of the moment about the TMJ axis in species with very hard and hard diets, the masseter was most important for species with soft diets, and the medial pterygoid was most important for species with liquid diets. 5. Our results highlight the utility of combining a modelling approach with in vivo data when conducting ecomorphological studies, and the importance of ecological classifications that reflect functional importance of performance traits.
Models of the mammalian masticatory apparatus predict that bite force is affected by both the degree of mouth opening (gape angle) and the location along the tooth row at which force is transferred (bite point). Theoretical analyses of gape angle and empirical studies of muscle function suggest that there is a trade-off between mechanical advantage and gape (Herring and Herring, 1974;Lindauer et al., 1993;Turkawski and van Eijden, 2001). For generalized mammals, larger gape angles require muscles to stretch and are predicted to negatively impact the geometry of their mechanical advantage. Among more specialized taxa, alterations in the geometry of muscle insertions and internal architecture over evolutionary time have resulted in species that can produce high bite forces at high gape angles (carnivores) and other species that are wellsuited to producing high bite forces at low gape angles (herbivores). With respect to bite point, models of the lower jaw as a simple class III lever or beam (e.g. Hylander, 1975;Radinsky, 1981;Weishampel, 1993) and constrained lever models that focus on protecting the temporomandibular joint from tensile loading (e.g. Greaves, 1978;Spencer, 1999) predict that bite forces increase at progressively posterior bite points. Constrained lever models further predict that bite forces level off and may decline posterior to an optimal bite point located at or near the first molar.Despite the widespread use of these models and predictions in discussions of mammalian feeding (e.g. Carraway et al., 1996;Dumont, 1997;Emerson and Radinsky, 1980;Freeman, 1981;Kiltie, 1982;Perez-Barberia and Gordon, 1999;Reduker, 1983;Sicuro and Oliveira, 2002;Stafford and Szalay, 2000), there are surprisingly few experimental data documenting bite force in non-human mammals. Data summarizing maximum bite forces elicited using electrical stimulation are available for macaques, opossums, and rats (Dechow and Carlson, 1983;Robins, 1977;Thomason et al., 1989). Natural, non-stimulated bite forces have been recorded at single (or combined) bite points in possums, hyenas, ferrets and bats (Aguirre et al., 2002;Binder and Van Valkenburgh, 2000;Dessem and Druzinsky, 1992;Thomason et al., 1989). Variation in non-stimulated bite force has been reported only for galagos and macaques (Hylander, 1977(Hylander, , 1979, in which there is a positive relationship between bite force and increasingly posterior bite point.Humans are the only mammals in which the combined effects of gape and bite point on non-stimulated bite force production have been studied in any detail. Even so, the integrated effects of bite point and gape angle on force production remain unclear (Spencer, 1999). Among experiments in which gape and bite point are altered Models of mammalian mastication predict that bite force is affected by both the degree of mouth opening (gape angle) and the point along the tooth row at which force is transferred to a food item (bite point). Despite the widespread use of these models in comparative analyses, experimental data do...
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
customersupport@researchsolutions.com
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
This site is protected by reCAPTCHA and the Google Privacy Policy and Terms of Service apply.
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.