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Extreme and rapid bursts of functional adaptations shape bite force in amniotes.

ABSTRACT: Adaptation is the fundamental driver of functional and biomechanical evolution. Accordingly, the states of biomechanical traits (absolute or relative trait values) have long been used as proxies for adaptations in response to direct selection. However, ignoring evolutionary history, in particular ancestry, passage of time and the rate of evolution, can be misleading. Here, we apply a recently developed phylogenetic statistical approach using significant rate shifts to detect instances of exceptional rates of adaptive changes in bite force in a large group of terrestrial vertebrates, the amniotes. Our results show that bite force in amniotes evolved through multiple bursts of exceptional rates of adaptive changes, whereby whole groups-including Darwin's finches, maniraptoran dinosaurs (group of non-avian dinosaurs including birds), anthropoids and hominins (fossil and modern humans)-experienced significant rate increases compared to the background rate. However, in most parts of the amniote tree of life, we find no exceptional rate increases, indicating that coevolution with body size was primarily responsible for the patterns observed in bite force. Our approach represents a template for future studies in functional morphology and biomechanics, where exceptional rates of adaptive changes can be quantified and potentially linked to specific ecological factors underpinning major evolutionary radiations.

SUBMITTER: Sakamoto M

PROVIDER: S-EPMC6367170 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Extreme and rapid bursts of functional adaptations shape bite force in amniotes.

Sakamoto Manabu M Ruta Marcello M Venditti Chris C

Proceedings. Biological sciences 20190101 1894

Adaptation is the fundamental driver of functional and biomechanical evolution. Accordingly, the states of biomechanical traits (absolute or relative trait values) have long been used as proxies for adaptations in response to direct selection. However, ignoring evolutionary history, in particular ancestry, passage of time and the rate of evolution, can be misleading. Here, we apply a recently developed phylogenetic statistical approach using significant rate shifts to detect instances of excepti ...[more]

PMID: 30963871

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Project description:Skeletal muscle mass, architecture and force-generating capacity are well known to scale with body size in animals, both throughout ontogeny and across species. Investigations of limb muscle scaling in terrestrial amniotes typically focus on individual muscles within select clades, but here this question was examined at the level of the whole limb across amniotes generally. In particular, the present study explored how muscle mass, force-generating capacity (measured by physiological cross-sectional area) and internal architecture (fascicle length) scales in the fore- and hindlimbs of extant mammals, non-avian saurians ('reptiles') and bipeds (birds and humans). Sixty species spanning almost five orders of magnitude in body mass were investigated, comprising previously published architectural data and new data obtained via dissections of the opossum Didelphis virginiana and the tegu lizard Salvator merianae. Phylogenetic generalized least squares was used to determine allometric scaling slopes (exponents) and intercepts, to assess whether patterns previously reported for individual muscles or functional groups were retained at the level of the whole limb, and to test whether mammals, reptiles and bipeds followed different allometric trajectories. In general, patterns of scaling observed in individual muscles were also observed in the whole limb. Reptiles generally have proportionately lower muscle mass and force-generating capacity compared to mammals, especially at larger body size, and bipeds exhibit strong to extreme positive allometry in the distal hindlimb. Remarkably, when muscle mass was accounted for in analyses of muscle force-generating capacity, reptiles, mammals and bipeds almost ubiquitously followed a single common scaling pattern, implying that differences in whole-limb force-generating capacity are principally driven by differences in muscle mass, not internal architecture. In addition to providing a novel perspective on skeletal muscle allometry in animals, the new dataset assembled was used to generate pan-amniote statistical relationships that can be used to predict muscle mass or force-generating capacity in extinct amniotes, helping to inform future reconstructions of musculoskeletal function in the fossil record.

Project description:BackgroundMeasuring mammals' bite force in laboratory conditions is not a simple task, let alone on wild medium-sized mammals in the field. Thus, morphometric-proxies are usually used to infer morphofunctional properties of musculoskeletal features. For instance, the study of bite force-indexes suggests that different capacities to crack food items reduce the competition between coexistent collared and white-lipped peccaries (Pecari tajacu and Tayassu pecari). The presence of exotic feral hogs (Sus scrofa) in peccaries' endemic areas gives rise to new ecological interactions between them. An example is the Brazilian Pantanal wetland, where ecomorphological mechanisms may play a role in their ecological relations. Taking this scenario as a case of study, we aimed to verify if the morphometric-proxies are de facto reliable tools, by comparing bite forces-indexes with the in vivo bite forces of these species.MethodsWe captured 21 collared and white-lipped peccaries and feral hogs in the Brazilian Pantanal to assess their bite force at first molar. The Bite Force Measuring Tube (BiTu) is a robust and simple mechanical device designed to be used in field conditions. Only 11 individuals successfully bit the BiTu before being released. Their body measurements were compared and correlated with their bite force. The in vivo bite forces were compared with bite force-indexes of two papers based on independent morphometric methods and datasets: Sicuro & Oliveira (2002) used classic morphometrics to infer the bite forces of these three species in the Brazilian Pantanal, and Hendges et al. (2019) used geometric morphometrics to compare bite forces-indexes and feeding habits of the extant peccary species. The results of all species were standardized (Z-curves) according to each method. Doing so, we obtained comparable dimensionless comparable values but maintaining the differences between them.ResultsThe morphometric-proxies-based studies presented similar results: collared peccaries present weaker bites than white-lipped peccaries and feral hogs, while these two species presented no significant differences in their bite force-indexes. The in vivo bite force results suggest the same relations predicted by the morphometric models, including the high variation among the feral hogs. We found a significant correlation between the individuals' weight (kg) and their actual bite force (N) but no significant correlations with the head length.ConclusionsThe BiTu proved to be a functional and low-cost tool to measure bite force in field conditions. The in vivo results presented a good correspondence with the predictions based on morphometric-proxies by Sicuro & Oliveira (2002) and Hendges et al. (2019). The results denote that these studies succeed in capturing the biomechanical signal of the three species' skull-jaw systems. This empirical validation confirms that these morphometric-proxies analyses are reliable methods to ecomorphological and evolutionary inferences.

Dataset Information

Extreme and rapid bursts of functional adaptations shape bite force in amniotes.

Publications

Extreme and rapid bursts of functional adaptations shape bite force in amniotes.

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