The arboreal environment is complex and irregular and imposes significant constraints on the locomotor ability of vertebrates, resulting in morphological adaptations. Carnivorans are of particular interest because they radiated several times independently into the arboreal milieu, leading to convergence in long bone anatomy. We investigated whether the forelimb muscles show differences in arboreal vs. terrestrial species and tested for convergence in muscle architecture. To do so, we studied the forelimb muscles in 17 species of carnivorans with different locomotor modes (arboreal and terrestrial). Our results showed that the forelimb musculature evolved in a convergent manner in arboreal species, resulting in more forceful and heavier wrist rotators and elbow flexors, even when accounting for phylogeny. This suggests that selective forces imposed by the environment drive the evolution of the muscular system towards a convergent phenotype that provides a functional advantage for locomotion in the complex threedimensional arboreal habitat.
Bite force is a key performance trait in lizards because biting is involved in many ecologically relevant tasks, including foraging, fighting and mating. Several factors have been suggested to impact bite force in lizards, such as head morphology (proximate factors), or diet, intraspecific competition and habitat characteristics (ultimate factors). However, these have been generally investigated separately and mostly at the interspecific level. Here we tested which factors drive variation in bite force at the population level and to what extent. Our study includes 20 populations of two closely related lacertid species, Podarcis melisellensis and Podarcis sicula, which inhabit islands in the Adriatic. We found that lizards with more forceful bites have relatively wider and taller heads, and consume more hard prey and plant material. Island isolation correlates with bite force, probably by driving resource availability. Bite force is only poorly explained by proxies of intraspecific competition. The linear distance from a large island and the proportion of difficult-to-reduce food items consumed are the ultimate factors that explain most of the variation in bite force. Our findings suggest that the way in which morphological variation affects bite force is species-specific, probably reflecting the different selective pressures operating on the two species.
Phenotypictraits have been shown to evolve in response to variation in the environment. However, the evolutionary processes underlying the emergence of phenotypic diversity can typically only be understood at the population level. Consequently, how subtle phenotypic differences at the intraspecific level can give rise to larger-scale changes in performance and ecology remains poorly understood. We here tested for the covariation between ecology, bite force, jaw muscle architecture, and the three-dimensional shape of the cranium and mandible in 16 insular populations of the lizards Podarcis melisellensis and P. sicula. We then compared the patterns observed at the among-population level with those observed at the interspecific level. We found that three-dimensional head shape as well as jaw musculature evolve similarly under similar ecological circumstances. Depending on the type of food consumed or on the level of sexual competition, different muscle groups were more developed and appeared to underlie changes in cranium and mandible shape. Our findings show that the local selective regimes are primary drivers of phenotypic variation resulting in predictable patterns of form and function. Moreover, intraspecific patterns of variation were generally consistent with those at the interspecific level, suggesting that microevolutionary variation may translate into macroevolutionary patterns of ecomorphological diversity.
Access to resources is a dynamic and multicausal process that determines the success and survival of a population. It is therefore often challenging to disentangle the factors affecting ecological traits like diet. Insular habitats provide a good opportunity to study how variation in diet originates, in particular in populations of mesopredators such as lizards. Indeed, high levels of population density associated with low food abundance and low predation are selection pressures typically observed on islands. In the present study, the diet of eighteen insular populations of two closely related species of lacertid lizards (Podarcis sicula and Podarcis melisellensis) was assessed. Our results reveal that despite dietary variability among populations, diet taxonomic diversity is not impacted by island area. In contrast, however, diet disparity metrics, based on the variability in the physical (hardness) and behavioral (evasiveness) properties of ingested food items, are correlated with island size. These findings suggest that an increase in intraspecific competition for access to resources may induce shifts in functional components of the diet. Additionally, the two species differed in the relation between diet disparity and island area suggesting that different strategies exist to deal with low food abundance in these two species. Finally, sexual dimorphism in diet and head dimensions is not greater on smaller islands, in contrast to our predictions.
Long bone inner structure and cross-sectional geometry display a strong functional signal, leading to convergences, and are widely analyzed in comparative anatomy at small and large taxonomic scales. Long bone microanatomical studies have essentially been conducted on transverse sections but also on a few longitudinal ones. Recent studies highlighted the interest in analyzing variations of the inner structure along the diaphysis using a qualitative as well as a quantitative approach. With the development of microtomography, it has become possible to study three-dimensional (3D) bone microanatomy and, in more detail, the form-function relationships of these features. This study focused on the selection of quantitative parameters to describe in detail the cross-sectional shape changes and distribution of the osseous tissue along the diaphysis. Two-dimensional (2D) virtual transverse sections were also performed in the two usual reference planes and results were compared with those obtained based on the whole diaphysis analysis. The sample consisted in 14 humeri and 14 femora of various mammalian taxa that are essentially terrestrial. Comparative quantitative analyses between different datasets made it possible to highlight the parameters that are strongly impacted by size and phylogeny and the redundant ones, and thus to estimate their relevance for use in form-function analyses. The analysis illustrated that results based on 2D transverse sections are similar for both sectional planes; thus if a strong bias exists when mixing sections from the two reference planes in the same analysis, it would not problematic to use either one plane or the other in comparative studies. However, this may no longer hold for taxa showing a much stronger variation in bone microstructure along the diaphysis. Finally, the analysis demonstrated the significant contribution of the parameters describing variations along the diaphysis, and thus the interest in performing 3D analyses; this should be even more fruitful for heterogeneous diaphyses. In addition, covariation analyses showed that there is a strong interest in removing the size effect to access the differences in the microstructure of the humerus and femur. This methodological study provides a reference for future quantitative analyses on long bone inner structure and should make it possible, through a detailed knowledge of each descriptive parameter, to better interpret results from the multivariate analyses associated with these studies. This will have direct implications for studies in vertebrate anatomy, but also in paleontology and anthropology.
Resource-limited environments may drive the rapid evolution of phenotypic traits and ecological preferences optimizing the exploitation of resources. Very small islands are often characterized by reduced food availability, seasonal fluctuations in resources and strong unpredictability. These features may drive the evolution of phenotypic traits such as high bite forces, allowing animals to exploit a wider variety of the available resources. They may also lead to more generalist dietary patterns in response to food scarcity. However, the lack of predators and competitors on such small islands often also leads to high densities and the evolution of strong sexual dimorphism, which may also drive the evolution of bite force. Here, we take advantage of a unique replicated introduction experiment to test whether lizards introduced into very small islands alter their feeding ecology and use different resources, resulting in the evolution of a large body size, large head size and large bite forces. Our results show that three years after their introduction, the island lizards were larger and had greater bite forces and more pronounced sexual dimorphism. However, the diets were only marginally different between animals from the source population on a very large nearby island and those on the islets. Moreover, distinct differences in diet between animals on the different islets were observed, suggesting that the local environment is a strong driver of resource use. Overall, lizards with absolutely and relatively (adjusted for body size) large bite forces did eat larger and harder prey. Taken together, our data suggest that intraspecific competition is an important driver of the rapid evolution of bite force, which may allow these lizards to exploit the scarce and fluctuating resources on the islets. Whether or not lizards will evolve to include other types of food such as plants in their diet, facilitated by their large bite forces, remains to be explored in future studies.
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