Cranial biomechanics in basal urodeles: the Siberian salamander (Salamandrella keyserlingii) and its evolutionary and developmental implications

Developmental changes in salamander skulls, before and after metamorphosis, afect the feeding capabilities of these animals. How changes in cranial morphology and tissue properties afect the function of the skull are key to decipher the early evolutionary history of the crown-group of salamanders. Here, 3D cranial biomechanics of the adult Salamandrella keyserlingii were analyzed under diferent tissue properties and ossifcation sequences of the cranial skeleton. This helped unravel that: (a) Mechanical properties of tissues (as bone, cartilage or connective tissue) imply a consensus between the stifness required to perform a function versus the fxation (and displacement) required with the surrounding skeletal elements. (b) Changes on the ossifcation pattern, producing fontanelles as a result of bone loss or failure to ossify, represent a trend toward simplifcation potentially helping to distribute stress through the skull, but may also imply a major destabilization of the skull. (c) Bone loss may be originated due to biomechanical optimization and potential reduction of developmental costs. (d) Hynobiids are excellent models for biomechanical reconstruction of extinct early urodeles

Evaluation of the functional capabilities of fins and limbs for moving on land: insights into the invasion of land by tetrapods

Transitions to novel habitats present different adaptive challenges, producing captivating examples of how functional innovations of the musculoskeletal system influence phenotypic divergence and adaptive radiations. One intriguing example is the transition from aquatic fishes to tetrapods. Recent technological advances and discoveries of critical fossils have catapulted our understanding on how fishes gave rise to terrestrial vertebrates. Considerable attention has been paid to legged locomotion on land, but given that the first tetrapods were aquatic, limbs did not evolve primarily for terrestriality. How, then, is the locomotor function of limbs different from fins? Extant amphibious fishes demonstrate that fins can be used on land, and anatomical analyses of the fish relatives of early stem tetrapods indicate that the appendicular bones of fishes could be quite robust. Consequently, there is a need to evaluate the ability of fins to withstand the physical challenges of terrestrial locomotion in order to shed light on how limbs conferred early stem tetrapods with an upper hand for becoming terrestrial. In the following papers, I have investigated the biomechanical capabilities of different musculoskeletal designs to understand the evolution of terrestrial locomotion in vertebrates. First, I compared the biomechanics of fins and limbs by measuring ground reaction force (GRF) production of mudskipper fishes (Periophthalmus barbarus) crutching and tiger salamanders (Ambystoma tigrinum) walking on level ground, two strategies for accomplishing terrestrial locomotion. Yet, tiger salamanders are already terrestrial. In order to understand how limbs function in a more habitually aquatic tetrapod, I conducted similar GRF analyses on a semi-aquatic newt (Pleurodeles waltl). Once tetrapods moved onto land, a major question is whether locomotion was primarily driven by the forelimbs or the hind limbs. Thus, I evaluated the ability of the forelimbs and hind limbs of A. tigrinum to withstand stresses during terrestrial locomotion. These data provided an opportunity to study whether the bones of different limbs possess different margins of safety against failure. Lastly, I synthesized how extant taxa can be used to model the biology of extinct taxa, advancing our knowledge about how functional innovation of the appendages contributed to one of the greatest revolutions in vertebrate history

A solution strategy to include the opening of the opercular slits in moving-mesh CFD models of suction feeding

The gill cover of fish and pre-metamorphic salamanders has a key role in suction feeding by acting as a one-way valve. It initially closes to avoid an inflow of water through the gill slits, after which it opens to allow outflow of the water that was sucked through the mouth into the expanded buccopharyngeal cavity. However, due to the inability of analytical models (relying on the continuity principle) to calculate a fluid flow through a shape-and-size-changing cavity with two openings, stringent boundary conditions had to be used in previously developed mathematical models after the moment of valve opening. By solving additionally for momentum conservation, computational fluid dynamics (CFD) has the capacity to dynamically simulate these flows, but this technique also faces complications to model a transition from closed to open valves. Here, I present a relatively simple solution strategy to incorporate valve opening, exemplified in an axisymmetrical model of a suction-feeding sunfish in ANSYS Fluent software. By controlling viscosity of a separately defined fluid entity at the opercular cavity region, early inflow can be blocked (high viscosity assigned) and later outflow can be allowed (changing viscosity to that of water). Finally, by analysing the CFD solution obtained for the sunfish model, a few new insights in the biomechanics of suction feeding will be discussed

Biomechanics and hydrodynamics of prey capture in the Chinese giant salamander reveal a high-performance jaw-powered suction feeding mechanism

During the evolutionary transition from fish to tetrapods, a shift from uni- to bidirectional suction feeding systems followed a reduction in the gill apparatus. Such a shift can still be observed during metamorphosis of salamanders, although many adult salamanders retain their aquatic lifestyle and feed by high-performance suction.Unfortunately, little is known about the interplay between jaws and hyobranchial motions to generate bidirectional suction flows. Here,we study the cranial morphology, aswell as kinematic and hydrodynamic aspects related to prey capture in the Chinese giant salamander (Andrias davidianus). Compared with fish and previously studied amphibians, A. davidianus uses an alternative suction mechanismthat mainly relies on accelerating water by separating the ‘plates’ formed by the long and broad upper and lower jaw surfaces. Computational fluid dynamics simulations, based on three-dimensional morphology and kinematical data from high-speed videos, indicate that the viscerocranial elements mainly serve to accommodate the water that was given a sufficient anterior-to-posterior impulse beforehand by powerful jawseparation.We hypothesize that this modifiedway of generating suction is primitive for salamanders, and that this behaviour could have played an important role in the evolution of terrestrial life in vertebrates by releasing mechanical constraints on the hyobranchial system

Comparative 3D analyses and palaeoecology of giant early amphibians (Temnospondyli: Stereospondyli)

Macroevolutionary, palaeoecological and biomechanical analyses in deep time offer the possibility to decipher the structural constraints, ecomorphological patterns and evolutionary history of extinct groups. Here, 3D comparative biomechanical analyses of the extinct giant early amphibian group of stereospondyls together with living lissamphibians and crocodiles, shows that: i) stereospondyls had peculiar palaeoecological niches with proper bites and stress patterns very different than those of giant salamanders and crocodiles; ii) their extinction may be correlated with the appearance of neosuchians, which display morphofunctional innovations. Stereospondyls weathered the end-Permian mass extinction, re-radiated, acquired gigantic sizes and dominated (semi) aquatic ecosystems during the Triassic. Because these ecosystems are today occupied by crocodilians, and stereospondyls are extinct amphibians, their palaeobiology is a matter of an intensive debate: stereospondyls were a priori compared with putative living analogous such as giant salamanders and/or crocodilians and our new results try to close this debate.Peer ReviewedPostprint (published version

Multi-Joint Analysis of Pose Viability Supports the Possibility of Salamander-Like Hindlimb Configurations in the Permian Tetrapod <i>Eryops megacephalus</i>

Synopsis Salamanders are often used as analogs for early tetrapods in paleontological reconstructions of locomotion. However, concerns have been raised about whether this comparison is justifiable, necessitating comparisons of a broader range of early tetrapods with salamanders. Here, we test whether the osteological morphology of the hindlimb in the early tetrapod (temnospondyl amphibian) Eryops megacephalus could have facilitated the sequence of limb configurations used by salamanders during terrestrial locomotion. To do so, we present a new method that enables the examination of full limb configurations rather than isolated joint poses. Based on this analysis, we conclude that E. megacephalus may indeed have been capable of salamander-like hindlimb kinematics. Our method facilitates the holistic visual comparison of limb configurations between taxa without reliance on the homology of coordinate system definitions, and can thus be applied to facilitate various comparisons between extinct and extant taxa, spanning the diversity of locomotion both past and present

Natural History Constrains the Macroevolution of Foot Morphology in European Plethodontid Salamanders

The natural history of organisms can have major effects on the tempo and mode of evolution, but few examples show how unique natural histories affect rates of evolution at macroevolutionary scales. European plethodontid salamanders (Plethodontidae: Hydromantes) display a particular natural history relative to other members of the family. Hydromantes commonly occupy caves and small crevices, where they cling to the walls and ceilings. On the basis of this unique and strongly selected behavior, we test the prediction that rates of phenotypic evolution will be lower in traits associated with climbing. We find that, within Hydromantes, foot morphological traits evolve at significantly lower rates than do other phenotypic traits. Additionally, Hydromantes displays a lower rate of foot morphology evolution than does a nonclimbing genus, Plethodon. Our findings suggest that macroevolutionary trends of phenotypic diversification can be mediated by the unique behavioral responses in taxa related to particular attributes of their natural history

Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae)

<p>Abstract</p> <p>Background</p> <p>A major goal in evolutionary biology is to understand the evolution of phenotypic diversity. Both natural and sexual selection play a large role in generating phenotypic adaptations, with biomechanical requirements and developmental mechanisms mediating patterns of phenotypic evolution. For many traits, the relative importance of selective and developmental components remains understudied.</p> <p>Results</p> <p>We investigated ontogenetic trajectories of foot morphology in the eight species of European plethodontid cave salamander to test the hypothesis that adult foot morphology was adapted for climbing. Using geometric morphometrics and other approaches, we found that developmental patterns in five species displayed little morphological change during growth (isometry), where the extensive interdigital webbing in adults was best explained as the retention of the juvenile morphological state. By contrast, three species exhibited significant allometry, with an increase in interdigital webbing during growth. Phylogenetic analyses revealed that multiple evolutionary transitions between isometry and allometry of foot webbing have occurred in this lineage. Allometric parameters of foot growth were most similar to those of a tropical species previously shown to be adapted for climbing. Finally, interspecific variation in adult foot morphology was significantly reduced as compared to variation among juveniles, indicating that ontogenetic convergence had resulted in a common adult foot morphology across species.</p> <p>Conclusions</p> <p>The results presented here provide evidence of a complex history of phenotypic evolution in this clade. The common adult phenotype exhibited among species reveals that selection plays an important part in generating patterns of foot diversity in the group. However, developmental trajectories arriving at this common morphology are distinct; with some species displaying developmental stasis (isometry), while others show an increase in foot webbing during growth. Thus, multiple developmental solutions exist to the same evolutionary challenge. Our findings underscore the importance of examining morphological adaptations from multiple perspectives, and emphasize that both selective hypotheses and developmental processes must be considered for a more comprehensive understanding of phenotypic evolution.</p

Reproducing Five Motor Behaviors in a Salamander Robot With Virtual Muscles and a Distributed CPG Controller Regulated by Drive Signals and Proprioceptive Feedback

Diverse locomotor behaviors emerge from the interactions between the spinal central pattern generator (CPG), descending brain signals and sensory feedback. Salamander motor behaviors include swimming, struggling, forward underwater stepping, and forward and backward terrestrial stepping. Electromyographic and kinematic recordings of the trunk show that each of these five behaviors is characterized by specific patterns of muscle activation and body curvature. Electrophysiological recordings in isolated spinal cords show even more diverse patterns of activity. Using numerical modeling and robotics, we explored the mechanisms through which descending brain signals and proprioceptive feedback could take advantage of the flexibility of the spinal CPG to generate different motor patterns. Adapting a previous CPG model based on abstract oscillators, we propose a model that reproduces the features of spinal cord recordings: the diversity of motor patterns, the correlation between phase lags and cycle frequencies, and the spontaneous switches between slow and fast rhythms. The five salamander behaviors were reproduced by connecting the CPG model to a mechanical simulation of the salamander with virtual muscles and local proprioceptive feedback. The main results were validated on a robot. A distributed controller was used to obtain the fast control loops necessary for implementing the virtual muscles. The distributed control is demonstrated in an experiment where the robot splits into multiple functional parts. The five salamander behaviors were emulated by regulating the CPG with two descending drives. Reproducing the kinematics of backward stepping and struggling however required stronger muscle contractions. The passive oscillations observed in the salamander's tail during forward underwater stepping could be reproduced using a third descending drive of zero to the tail oscillators. This reduced the drag on the body in our hydrodynamic simulation. We explored the effect of local proprioceptive feedback during swimming and forward terrestrial stepping. We found that feedback could replace or reduce the need for different drives in both cases. It also reduced the variability of intersegmental phase lags toward values appropriate for locomotion. Our work suggests that different motor behaviors do not require different CPG circuits: a single circuit can produce various behaviors when modulated by descending drive and sensory feedback

Palate anatomy and morphofunctional aspects of interpterygoid vacuities in temnospondyl cranial evolution

Temnospondyls were the morphologically and taxonomically most diverse group of early tetrapods with a near-global distribution during the Palaeozoic and Mesozoic. Members of this group occupied a range of different habitats (aquatic, amphibious, terrestrial), reflected by large morphological disparity of the cranium throughout their evolutionary history. A diagnostic feature of temnospondyls is the presence of an open palate with large interpterygoid vacuities, in contrast to the closed palate of most other early tetrapods and their fish-like relatives. Although the function of the interpterygoid vacuities has been discussed in the past, no quantitative studies have been performed to assess their biomechanical significance. Here, we applied finite element analysis, to test the possibility that the interpterygoid vacuities served for stress distribution during contraction of the jaw closing musculature. Different original and theoretical skull models, in which the vacuities differed in size or were completely absent, were compared for their mechanical performance. Our results demonstrate that palatal morphology played a considerable role in cranial biomechanics of temnospondyls. The presence of large cranial vacuities were found to offer the dual benefit of providing additional muscle attachment areas and allowing for more effective force transmission and thus an increase in bite force without compromising cranial stability