Maximum trunk tip force assessment related to trunk position and prehensile 'fingers' implication in African savannah elephants.

African elephants have a wide range of abilities using their trunk. As a muscular hydrostat, and thanks to the two finger-like processes at its tip, this proboscis can both precisely grasp and exert considerable force by wrapping. Yet few studies have attempted to quantify its distal grasping force. Thus, using a device equipped with force sensors and an automatic reward system, the trunk tip pinch force has been quantified in five captive female African savanna elephants. Results showed that the maximum pinch force of the trunk was 86.4 N, which may suggest that this part of the trunk is mainly dedicated to precision grasping. We also highlighted for the first time a difference in force between the two fingers of the trunk, with the dorsal finger predominantly stronger than the ventral finger. Finally, we showed that the position of the trunk, particularly the torsion, influences its force and distribution between the two trunk fingers. All these results are discussed in the light of the trunk's anatomy, and open up new avenues for evolutionary reflection and soft robot grippers.

Show Me Your Teeth And I Will Tell You What You Eat: Differences in Tooth Enamel in Snakes with Different Diets.

Teeth are composed of the hardest tissues in the vertebrate body and have been studied extensively to infer diet in vertebrates. The morphology and structure of enamel is thought to reflect feeding ecology. Snakes have a diversified diet, some species feed on armored lizards, others on soft invertebrates. Yet, little is known about how tooth enamel, and specifically its thickness, is impacted by diet. In this study, we first describe the different patterns of enamel distribution and thickness in snakes. Then, we investigate the link between prey hardness and enamel thickness and morphology by comparing the dentary teeth of 63 species of snakes. We observed that the enamel is deposited asymmetrically at the antero-labial side of the tooth. Both enamel coverage and thickness vary a lot in snakes, from species with thin enamel, only at the tip of the tooth to a full facet covered with enamel. There variations are related with prey hardness: snakes feeding on hard prey have a thicker enamel and a lager enamel coverage while species. Snakes feeding on softer prey have a thin enamel layer confined to the tip of the tooth.

Armed to the teeth: The underestimated diversity in tooth shape in snakes and its relation to feeding behavior and diet.

The structure, composition, and shape of teeth have been related to dietary specialization in many vertebrate species, but comparative studies on snakes' teeth are lacking. Yet, snakes have diverse dietary habits that may impact the shape of their teeth. We hypothesize that prey properties, such as hardness and shape, as well as feeding behavior, such as aquatic or arboreal predation, or holding vigorous prey, impose constraints on the evolution of tooth shape in snakes. We compared the morphology of the dentary teeth of 63 species that cover the phylogenetic and dietary diversity of snakes, using 3D geometric morphometrics and linear measurements. Our results show that prey hardness, foraging substrate, and the main feeding mechanical challenge are important drivers of tooth shape, size, and curvature. Overall, long, slender, curved teeth with a thin layer of hard tissue are observed in species that need to maintain a grip on their prey. Short, stout, less curved teeth are associated with species that undergo high or repeated loads. Our study demonstrates the diversity of tooth morphology in snakes and the need to investigate its underlying functional implications to better understand the evolution of teeth in vertebrates.

Shape variation in the limb long bones of modern elephants reveals adaptations to body mass and habitat.

During evolution, several vertebrate lineages have shown trends towards an increase in mass. Such a trend is associated with physiological and musculoskeletal changes necessary to carry and move an increasingly heavy body. Due to their prominent role in the support and movement of the body, limb long bones are highly affected by these shifts in body mass. Elephants are the heaviest living terrestrial mammals, displaying unique features allowing them to withstand their massive weight, such as the columnarity of their limbs, and as such are crucial to understand the evolution towards high body mass in land mammals. In this study, we investigate the shape variation of the six limb long bones among the modern elephants, Elephas maximus and Loxodonta africana, to understand the effect of body mass and habitat on the external anatomy of the bones. To do so, we use three-dimensional geometric morphometrics (GMMs) and qualitative comparisons to describe the shape variation, at both the intraspecific and interspecific levels. Our results reveal that the two species share similar negative ontogenetic allometric patterns (i.e. becoming stouter with increased length) in their humerus and femur, but not in the other bones: the proximal epiphyses of the stylopod bones develop considerably during growth, while the distal epiphyses, which are involved in load distribution in the elbow and knee joints, are already massive in juveniles. We attribute this pattern to a weight-bearing adaptation already present in young specimens. Among adults of the same species, bone robustness increases with body mass, so that heavier specimens display stouter bones allowing for a better mechanical load distribution. While this robustness variation is significant for the humerus only, all the other bones appear to follow the same pattern. This is particularly visible in the ulna and tibia, but less so in the femur, which suggests that the forelimb and hindlimb adapted differently to high body mass support. Robustness analyses, while significant for the humerus only, suggest more robust long bones in Asian elephants than in African savanna elephants. More specifically, GMMs and qualitative comparisons indicate that three bones are clearly distinct when comparing the two species: in E. maximus the humerus, the ulna and the tibia display enlarged areas of muscular insertions for muscles involved in joint and limb stabilization, as well as in limb rotation. These results suggest a higher limb compliance in Asian elephants, associated with a higher dexterity, which could be linked to their habitat and foraging habits.

Comparative morpho-functional analysis of the humerus and ulna in three Western European moles species of the genus Talpa, including the newly described T. aquitania.

The forelimb is involved in many behaviours including locomotion. Notably, the humero-ulnar articulation, implicated in the elbow joint, is of particular importance for both mobility and stability. Functional constraints, induced in part by environmental plasticity, are thought to drive an important part of the bone shape as bone directly responds and remodels in response to both muscle and external forces. In this context, the study of subterranean moles is of particular interest. These moles occupy a hard and heavy medium in comparison with air or water, requiring a powerful body structure to shear and shift the soil. Their general morphology is therefore adapted to digging and to their subterranean lifestyle. The various morpho-functional patterns, which drive diverse abilities according to the environment, are likely targets of natural selection and it is, therefore, useful to understand the relationships between the bone shape and their function. Here, we quantify, through 3D geometric morphometric methods, the interspecific variability in the morphology of the ulna and humerus of three Talpa species, including the new species Talpa aquitania, to infer their potential consequence in species digging performance. We also quantify shape covariation and morphological integration between the humerus and the ulna to test whether these bones evolve as a uniform functional unit or as more or less independent modules. Our results show that interspecific anatomical differences in the humerus and ulna exist among the three species. Shape changes are mostly located at the level of joints and muscle attachments. As the species tend to live in allopatry and the fossorial lifestyle induces strong ecological constraints, interspecific variations could be explained by the properties of the environment in which they live, such as the compactness of the soil. Our results also show that the humerus and ulna are highly integrated. The covariation between the humerus and ulna in moles is dominated by variation in the attachment areas and particularly of the attachment areas of shoulder muscles concerning the humerus, which affect the mechanical force deployed during locomotion and digging. This study also highlights that in the new species, T. aquitania, variations in anatomical structure (general shape and joints) exist and are related to the locality of collect of the individuals.

Measuring the force of the tip of the elephants trunk.

Forces that animals can exert is of great interest in biology. Regarding the elephant trunk, the maximum mass that an elephant can lift with its trunk is known, but the pinching force of the trunk tip is unknown. We here present an original system to measure this force for an organ much coveted in soft robotics for example. It consists of:•A wooden box protecting the elephants and the measuring system with no protruding parts except the sensor. This box has an opening at the back to fill it with apples and a trap door at the front to release the apples.•Two load cells protruding from the box connected to an electronic system controlled by an Arduino card that records and sends the pinch force via Wi-Fi to a laptop while releasing a reward apple.•Depending on the threshold chosen, the elephant must pinch harder than the previous time to release the next apple. The repetition of this action allows us to approach the maximum force it can achieve.The system, tested on elephants at the Beauval Zooparc (France), has demonstrated that it is effective in measuring the pinching force of the tip of the trunk.

Modifications of the locomotor system in habitually quadrupedal humans.

The acquisition of habitual bipedal locomotion, which resulted in numerous modifications of the skeleton was a crucial step in hominid evolution. However, our understanding of the inherited skeletal modifications versus those acquired while learning to walk remains limited. We here present data derived from X-rays and CT scans of quadrupedal adult humans and compare the morphology of the vertebral column, pelvis and femur to that of a bipedal brother. We show how a skeleton forged by natural selection for bipedal locomotion is modified when used to walk quadrupedally. The quadrupedal brother is characterised by the absence of femoral obliquity, a very high anteversion angle of the femoral neck, a very high collo-diaphyseal angle and a very reduced lordosis. The differences in the pelvis are more subtle and complex, yet of functional importance. The modification of the ischial spines to an ischial ridge and the perfectly rounded shape of the sacral curvature are two unique features that can be directly attributed to a quadrupedal posture and locomotion. We propose a functional interpretation of these two exceptional modifications. Unexpectedly, the quadrupedal brother and sister show a greater angle of pelvic incidence compared to their bipedal brother, a trait previously shown to increase with learning to walk in bipedal subjects. Moreover, the evolution from an occasional towards a permanent bipedality has given rise to a functional association between the angle of pelvic incidence and the lumbar curvature, with high angles of incidence and greater lumbar curvature promoting stability during bipedal locomotion. The quadrupedal brother and sister with a high angle of incidence and a very reduced lordosis thus show a complete decoupling of this complex functional integration.

Incongruences between morphology and molecular phylogeny provide an insight into the diversification of the Crocidura poensis species complex.

Untangling the factors of morphological evolution has long held a central role in the study of evolutionary biology. Extant speciose clades that have only recently diverged are ideal study subjects, as they allow the examination of rapid morphological variation in a phylogenetic context, providing insights into a clade's evolution. Here, we focus on skull morphological variability in a widely distributed shrew species complex, the Crocidura poensis species complex. The relative effects of taxonomy, size, geography, climate and habitat on skull form were tested, as well as the presence of a phylogenetic signal. Taxonomy was the best predictor of skull size and shape, but surprisingly both size and shape exhibited no significant phylogenetic signal. This paper describes one of the few cases within a mammal clade where morphological evolution does not match the phylogeny. The second strongest predictor for shape variation was size, emphasizing that allometry can represent an easily accessed source of morphological variability within complexes of cryptic species. Taking into account species relatedness, habitat preferences, geographical distribution and differences in skull form, our results lean in favor of a parapatric speciation model within this complex of species, where divergence occurred along an ecological gradient, rather than a geographic barrier.

Modeling intervertebral articulation: The rotule à doigt mechanical joint (RAD) in birds and mammals.

The vertebrate skeleton is composed of articulated bones. Most of the articulations are classically described using mechanical joints, except the intervertebral joint. The aim of this study was to identify a joint model with the same mechanical features as the cervical joints. On the neck vertebrae, six articular surfaces participate in the joint: the cranial part of the centrum and the facets of the two prezygapophyses of a vertebra articulate on the caudal part of the centrum and the two articular facets of the postzygapophyses of the previous vertebra. We used the intervertebral joints of the birds neck to identify the mechanical joint representing intervertebral linkage. This link was described in the literature as a joint allowing two or three rotations and no translation. These features correspond to the rotule à doigt (RAD) joint, a ball and socket joint with a pin. We compared the RAD joint to the postaxial intervertebral joints of the avian neck and found it a suitable model to determine the geometrical features involved in the joint mobility. The difference in the angles of virtual axes linking the geometrical center of the centrum to the zygapophysis surfaces determines the mean dorsoventral flexion of the joint. It also helps to limit longitudinal rotation. The orientation of the zygapophysis surfaces determines the range of motion in both dorsoventral and lateral flexion. The overall system prevents dislocation. The model was validated on 13 joints of a vulture neck and 11 joints of a swallow neck and on one joint (C6-C7) in each of three mammal species: the wolf (Canis lupus), mole (Talpa europaea), and human (Homo sapiens). The RAD mechanical joint was found in all vertebral articulations. This validation of the model on different species shows that the RAD intervertebral joint model makes it possible to extract the parameters that guide and limit the mobility of the cervical spine from the complex shape of the vertebrae and to compare them in interspecific studies.

Underwater photogrammetry for close-range 3D imaging of dry-sensitive objects: The case study of cephalopod beaks.

Technical advances in 3D imaging have contributed to quantifying and understanding biological variability and complexity. However, small, dry-sensitive objects are not easy to reconstruct using common and easily available techniques such as photogrammetry, surface scanning, or micro-CT scanning. Here, we use cephalopod beaks as an example as their size, thickness, transparency, and dry-sensitive nature make them particularly challenging. We developed a new, underwater, photogrammetry protocol in order to add these types of biological structures to the panel of photogrammetric possibilities.We used a camera with a macrophotography mode in a waterproof housing fixed in a tank with clear water. The beak was painted and fixed on a colored rotating support. Three angles of view, two acquisitions, and around 300 pictures per specimen were taken in order to reconstruct a full 3D model. These models were compared with others obtained with micro-CT scanning to verify their accuracy.The models can be obtained quickly and cheaply compared with micro-CT scanning and have sufficient precision for quantitative interspecific morphological analyses. Our work shows that underwater photogrammetry is a fast, noninvasive, efficient, and accurate way to reconstruct 3D models of dry-sensitive objects while conserving their shape. While the reconstruction of the shape is accurate, some internal parts cannot be reconstructed with photogrammetry as they are not visible. In contrast, these structures are visible using reconstructions based on micro-CT scanning. The mean difference between both methods is very small (10-5 to 10-4 mm) and is significantly lower than differences between meshes of different individuals.This photogrammetry protocol is portable, easy-to-use, fast, and reproducible. Micro-CT scanning, in contrast, is time-consuming, expensive, and nonportable. This protocol can be applied to reconstruct the 3D shape of many other dry-sensitive objects such as shells of shellfish, cartilage, plants, and other chitinous materials.

Correction to 'Limited thermal plasticity and geographical divergence in the ovipositor of Drosophila suzukii'.

[This corrects the article DOI: 10.1098/rsos.191577.].

Limited thermal plasticity and geographical divergence in the ovipositor of Drosophila suzukii.

Phenotypic plasticity has been repeatedly suggested to facilitate adaptation to new environmental conditions, as in invasions. Here, we investigate this possibility by focusing on the worldwide invasion of Drosophila suzukii: an invasive species that has rapidly colonized all continents over the last decade. This species is characterized by a highly developed ovipositor, allowing females to lay eggs through the skin of ripe fruits. Using a novel approach based on the combined use of scanning electron microscopy and photogrammetry, we quantified the ovipositor size and three-dimensional shape, contrasting invasive and native populations raised at three different developmental temperatures. We found a small but significant effect of temperature and geographical origin on the ovipositor shape, showing the occurrence of both geographical differentiation and plasticity to temperature. The shape reaction norms are in turn strikingly similar among populations, suggesting very little difference in shape plasticity among invasive and native populations, and therefore rejecting the hypothesis of a particular role for the plasticity of the ovipositor in the invasion success. Overall, the ovipositor shape seems to be a fairly robust trait, indicative of stabilizing selection. The large performance spectrum rather than the flexibility of the ovipositor would thus contribute to the success of D. suzukii worldwide invasion.