The respiratory system influences flight mechanics in soaring birds.

The subpectoral diverticulum (SPD) is an extension of the respiratory system in birds that is located between the primary muscles responsible for flapping the wing1,2. Here we survey the pulmonary apparatus in 68 avian species, and show that the SPD was present in virtually all of the soaring taxa investigated but absent in non-soarers. We find that this structure evolved independently with soaring flight at least seven times, which indicates that the diverticulum might have a functional and adaptive relationship with this flight style. Using the soaring hawks Buteo jamaicensis and Buteo swainsoni as models, we show that the SPD is not integral for ventilation, that an inflated SPD can increase the moment arm of cranial parts of the pectoralis, and that pectoralis muscle fascicles are significantly shorter in soaring hawks than in non-soaring birds. This coupling of an SPD-mediated increase in pectoralis leverage with force-specialized muscle architecture produces a pneumatic system that is adapted for the isometric contractile conditions expected in soaring flight. The discovery of a mechanical role for the respiratory system in avian locomotion underscores the functional complexity and heterogeneity of this organ system, and suggests that pulmonary diverticula are likely to have other undiscovered secondary functions. These data provide a mechanistic explanation for the repeated appearance of the SPD in soaring lineages and show that the respiratory system can be co-opted to provide biomechanical solutions to the challenges of flight and thereby influence the evolution of avian volancy.

Convergent evolution of quadrupedality in ornithischian dinosaurs was achieved through disparate forelimb muscle mechanics.

The secondary evolution of quadrupedality from bipedal ancestry is a rare evolutionary transition in tetrapods yet occurred convergently at least three times within ornithischian dinosaurs. Despite convergently evolving quadrupedal gait, ornithischians exhibited variable anatomy, particularly in the forelimbs, which underwent a major functional change from assisting in foraging and feeding in bipeds to becoming principal weight-bearing components of the locomotor system in quadrupeds. Here, we use three-dimensional multi-body dynamics models to demonstrate quantitatively that different quadrupedal ornithischian clades evolved distinct forelimb musculature, particularly around the shoulder. We find that major differences in glenohumeral abduction-adduction and long axis rotation muscle leverages were key drivers of mechanical disparity, thereby refuting previous hypotheses about functional convergence in major clades. Elbow muscle leverages were also disparate across the major ornithischian lineages, although high elbow extension muscle leverages were convergent between most quadrupeds. Unlike in ornithischian hind limbs, where differences are more closely tied to functional similarity than phylogenetic relatedness, mechanical disparity in ornithischian forelimbs appears to have been shaped primarily by phylogenetic constraints. Differences in ancestral bipedal taxa within each clade may have resulted in disparate ecomorphological constraints on the evolutionary pathways driving divergence in their quadrupedal descendants.

Skeletal muscle function underpins muscle spindle abundance.

Muscle spindle abundance is highly variable within and across species, but we currently lack any clear picture of the mechanistic causes or consequences of this variation. Previous use of spindle abundance as a correlate for muscle function implies a mechanical underpinning to this variation, but these ideas have not been tested. Herein, we use integrated medical imaging and subject-specific musculoskeletal models to investigate the relationship between spindle abundance, muscle architecture and in vivo muscle behaviour in the human locomotor system. These analyses indicate that muscle spindle number is tightly correlated with muscle fascicle length, absolute fascicle length change, velocity of fibre lengthening and active muscle forces during walking. Novel correlations between functional indices and spindle abundance are also recovered, where muscles with a high abundance predominantly function as springs, compared to those with a lower abundance mostly functioning as brakes during walking. These data demonstrate that muscle fibre length, lengthening velocity and fibre force are key physiological signals to the central nervous system and its modulation of locomotion, and that muscle spindle abundance may be tightly correlated to how a muscle generates work. These insights may be combined with neuromechanics and robotic studies of motor control to help further tease apart the functional drivers of muscle spindle composition.

Evolutionary biomechanics: hard tissues and soft evidence?

Biomechanical modelling is a powerful tool for quantifying the evolution of functional performance in extinct animals to understand key anatomical innovations and selective pressures driving major evolutionary radiations. However, the fossil record is composed predominantly of hard parts, forcing palaeontologists to reconstruct soft tissue properties in such models. Rarely are these reconstruction approaches validated on extant animals, despite soft tissue properties being highly determinant of functional performance. The extent to which soft tissue reconstructions and biomechanical models accurately predict quantitative or even qualitative patterns in macroevolutionary studies is therefore unknown. Here, we modelled the masticatory system in extant rodents to objectively test the ability of current muscle reconstruction methods to correctly identify quantitative and qualitative differences between macroevolutionary morphotypes. Baseline models generated using measured soft tissue properties yielded differences in muscle proportions, bite force, and bone stress expected between extant sciuromorph, myomorph, and hystricomorph rodents. However, predictions from models generated using reconstruction methods typically used in fossil studies varied widely from high levels of quantitative accuracy to a failure to correctly capture even relative differences between macroevolutionary morphotypes. Our novel experiment emphasizes that correctly reconstructing even qualitative differences between taxa in a macroevolutionary radiation is challenging using current methods. Future studies of fossil taxa should incorporate systematic assessments of reconstruction error into their hypothesis testing and, moreover, seek to expand primary datasets on muscle properties in extant taxa to better inform soft tissue reconstructions in macroevolutionary studies.

Evolutionary versatility of the avian neck.

Bird necks display unparalleled levels of morphological diversity compared to other vertebrates, yet it is unclear what factors have structured this variation. Using three-dimensional geometric morphometrics and multivariate statistics, we show that the avian cervical column is a hierarchical morpho-functional appendage, with varying magnitudes of ecologically driven osteological variation at different scales of organization. Contrary to expectations given the widely varying ecological functions of necks in different species, we find that regional modularity of the avian neck is highly conserved, with an overall structural blueprint that is significantly altered only by the most mechanically demanding ecological functions. Nevertheless, the morphologies of vertebrae within subregions of the neck show more prominent signals of adaptation to ecological pressures. We also find that both neck length allometry and the nature of neck elongation in birds are different from other vertebrates. In contrast with mammals, neck length scales isometrically with head mass and, contrary to previous work, we show that neck elongation in birds is achieved predominantly by increasing vertebral lengths rather than counts. Birds therefore possess a cervical spine that may be unique in its versatility among extant vertebrates, one that, since the origin of flight, has adapted to function as a surrogate forelimb in varied ecological niches.

Foot anatomy, walking energetics, and the evolution of human bipedalism.

Interspecies differences in locomotor efficiency have been extensively researched, but within-species variation in the metabolic cost of walking and its underlying causes have received much less attention. This is somewhat surprising given the importance of walking energetics to natural selection, and the fact that the mechanical efficiency of striding bipedalism in modern humans is thought to be related in some part to the unique morphology of the human foot. Previous studies of human running have linked specific anatomical traits in the foot to variations in locomotor energetics to provide insight into form-function relationships in human evolution. However, such studies are relatively rare, particularly for walking. In this study, relationships between a range of functional musculoskeletal traits in the human lower limb and the energetics of walking over compliant and noncompliant substrates are examined, with particular focus on the lower limb and foot. Twenty-nine young, healthy individuals walked across three surfaces-a noncompliant laboratory floor, and compliant 6 cm and 13 cm thick foams-at self-selected speeds while oxygen consumption was measured, from which the metabolic cost of transport was calculated. Lower limb lengths, calcaneus lengths, foot shape indices, and maximum isometric plantarflexion torques were also measured and subsequently tested for relationships with metabolic cost over these surfaces using linear regression. It was found that metabolic cost varied considerably between individuals within and across substrate types, but this variation was not statistically related to or explained by variations in musculoskeletal parameters considered to be adaptively important to efficient bipedal locomotion. This therefore provides no supportive evidence that variations in these gross anatomical parameters confer significant advantages to the efficiency of walking, and therefore suggest caution in the use of similar metrics to infer differences in walking energetics in closely related fossil species.

Subject-specific muscle properties from diffusion tensor imaging significantly improve the accuracy of musculoskeletal models.

Musculoskeletal modelling is an important platform on which to study the biomechanics of morphological structures in vertebrates and is widely used in clinical, zoological and palaeontological fields. The popularity of this approach stems from the potential to non-invasively quantify biologically important but difficult-to-measure functional parameters. However, while it is known that model predictions are highly sensitive to input values, it is standard practice to build models by combining musculoskeletal data from different sources resulting in 'generic' models for a given species. At present, there are little quantitative data on how merging disparate anatomical data in models impacts the accuracy of these functional predictions. This issue is addressed herein by quantifying the accuracy of both subject-specific human limb models containing individualised muscle force-generating properties and models built using generic properties from both elderly and young individuals, relative to experimental muscle torques obtained from an isokinetic dynamometer. The results show that subject-specific models predict isokinetic muscle torques to a greater degree of accuracy than generic models at the ankle (root-mean-squared error - 7.9% vs. 49.3% in elderly anatomy-based models), knee (13.2% vs. 57.3%) and hip (21.9% vs. 32.8%). These results have important implications for the choice of musculoskeletal properties in future modelling studies, and the relatively high level of accuracy achieved in the subject-specific models suggests that such models can potentially address questions about inter-subject variations of muscle functions. However, despite relatively high levels of overall accuracy, models built using averaged generic muscle architecture data from young, healthy individuals may lack the resolution and accuracy required to study such differences between individuals, at least in certain circumstances. The results do not wholly discourage the continued use of averaged generic data in musculoskeletal modelling studies but do emphasise the need for to maximise the accuracy of input values if studying intra-species form-function relationships in the musculoskeletal system.

Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs.

Locomotion in living birds (Neornithes) has two remarkable features: feather-assisted flight, and the use of unusually crouched hindlimbs for bipedal support and movement. When and how these defining functional traits evolved remains controversial. However, the advent of computer modelling approaches and the discoveries of exceptionally preserved key specimens now make it possible to use quantitative data on whole-body morphology to address the biomechanics underlying this issue. Here we use digital body reconstructions to quantify evolutionary trends in locomotor biomechanics (whole-body proportions and centre-of-mass position) across the clade Archosauria. We use three-dimensional digital reconstruction to estimate body shape from skeletal dimensions for 17 archosaurs along the ancestral bird line, including the exceptionally preserved, feathered taxa Microraptor, Archaeopteryx, Pengornis and Yixianornis, which represent key stages in the evolution of the avian body plan. Rather than a discrete transition from more-upright postures in the basal-most birds (Avialae) and their immediate outgroup deinonychosauria, our results support hypotheses of a gradual, stepwise acquisition of more-crouched limb postures across much of theropod evolution, although we find evidence of an accelerated change within the clade Maniraptora (birds and their closest relatives, such as deinonychosaurs). In addition, whereas reduction of the tail is widely accepted to be the primary morphological factor correlated with centre-of-mass position and, hence, evolution of hindlimb posture, we instead find that enlargement of the pectoral limb and several associated trends have a much stronger influence. Intriguingly, our support for the onset of accelerated morpho-functional trends within Maniraptora is closely correlated with the evolution of flight. Because we find that the evolution of enlarged forelimbs is strongly linked, via whole-body centre of mass, to hindlimb function during terrestrial locomotion, we suggest that the evolution of avian flight is linked to anatomical novelties in the pelvic limb as well as the pectoral.

A Three-Dimensional Musculoskeletal Model of the Western Lowland Gorilla Foot: Examining Muscle Torques and Function.

Due to difficulty of obtaining accurate quantitative data on foot muscles, relatively little has been done to study foot muscle function in non-human apes. Gorilla feet are known to be similar in bony proportions and mechanics to those of humans, hence are key to understanding human foot evolution and its ecological context. We present the first 3D musculoskeletal computer model of a western lowland gorilla foot, giving muscle torques about the tarsometatarsal, metatarsophalangeal and interphalangeal joints of digits 2-5. Peak flexor torque around the fifth metatarsophalangeal joint occurs at a highly flexed position, suggesting an ability to maintain flexed postures around lateral metatarsophalangeal joints, useful for grasping vertical supports. For distal interphalangeal joints, flexor torques peaked the more medial the digit at relatively flexed postures. We report, for the first time, interossei acting upon proximal and distal interphalangeal joints. All these facilitate maintenance of flexed positions around distal interphalangeal joints, likely used for grasping of small supports/objects. Humans lack these features, suggesting that semi-arboreal early hominins made less use of the peripheral canopy than gorillines. Information here could be used in gorilla enclosure design to encourage wild-type locomotor repertoires in captivity.

The importance of muscle architecture in biomechanical reconstructions of extinct animals: a case study using Tyrannosaurus rex.

Functional reconstructions of extinct animals represent a crucial step towards understanding palaeocological interactions, selective pressures and macroevolutionary patterns in the fossil record. In recent years, computational approaches have revolutionised the field of 'evolutionary biomechanics' and have, in general, resulted in convergence of quantitative estimates of performance on increasingly narrow ranges for well studied taxa. Studies of body mass and locomotor performance of Tyrannosaurus rex - arguably the most intensively studied extinct animal - typify this pattern, with numerous independent studies predicting similar body masses and maximum locomotor speeds for this animal. In stark contrast to this trend, recent estimates of maximum bite force in T. rex vary considerably (> 50%) despite use of similar quantitative methodologies. Herein we demonstrate that the mechanistic causes of these disparate predictions are indicative of important and underappreciated limiting factors in biomechanical reconstructions of extinct organisms. Detailed comparison of previous models of T. rex bite force reveals that estimations of muscle fibre lengths and architecture are the principal source of disagreement between studies, and therefore that these parameters represents the greatest source of uncertainty in these reconstructions, and potentially therefore extinct animals generally. To address the issue of fibre length and architecture estimation in extinct animals we present data tabulated from the literature of muscle architecture from over 1100 muscles measured in extant terrestrial animals. Application of this dataset in a reanalysis of T. rex bite force emphasises the need for more data on jaw musculature from living carnivorous animals, alongside increased sophistication of modelling approaches. In the latter respect we predict that implementing limits on skeletal loading into musculoskeletal models will narrow predictions for T. rex bite force by excluding higher-end estimates.

Open data and digital morphology.

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.

A quantitative evaluation of physical and digital approaches to centre of mass estimation.

Centre of mass is a fundamental anatomical and biomechanical parameter. Knowledge of centre of mass is essential to inform studies investigating locomotion and other behaviours, through its implications for segment movements, and on whole body factors such as posture. Previous studies have estimated centre of mass position for a range of organisms, using various methodologies. However, few studies assess the accuracy of the methods that they employ, and often provide only brief details on their methodologies. As such, no rigorous, detailed comparisons of accuracy and repeatability within and between methods currently exist. This paper therefore seeks to apply three methods common in the literature (suspension, scales and digital modelling) to three 'calibration objects' in the form of bricks, as well as three birds to determine centre of mass position. Application to bricks enables conclusions to be drawn on the absolute accuracy of each method, in addition to comparing these results to assess the relative value of these methodologies. Application to birds provided insights into the logistical challenges of applying these methods to biological specimens. For bricks, we found that, provided appropriate repeats were conducted, the scales method yielded the most accurate predictions of centre of mass (within 1.49 mm), closely followed by digital modelling (within 2.39 mm), with results from suspension being the most distant (within 38.5 mm). Scales and digital methods both also displayed low variability between centre of mass estimates, suggesting they can accurately and consistently predict centre of mass position. Our suspension method resulted not only in high margins of error, but also substantial variability, highlighting problems with this method.

A 3D musculoskeletal model of the western lowland gorilla hind limb: moment arms and torque of the hip, knee and ankle.

Three-dimensional musculoskeletal models have become increasingly common for investigating muscle moment arms in studies of vertebrate locomotion. In this study we present the first musculoskeletal model of a western lowland gorilla hind limb. Moment arms of individual muscles around the hip, knee and ankle were compared with previously published data derived from the experimental tendon travel method. Considerable differences were found which we attribute to the different methodologies in this specific case. In this instance, we argue that our 3D model provides more accurate and reliable moment arm data than previously published data on the gorilla because our model incorporates more detailed consideration of the 3D geometry of muscles and the geometric constraints that exist on their lines-of-action about limb joints. Our new data have led us to revaluate the previous conclusion that muscle moment arms in the gorilla hind limb are optimised for locomotion with crouched or flexed limb postures. Furthermore, we found that bipedalism and terrestrial quadrupedalism coincided more regularly with higher moment arms and torque around the hip, knee and ankle than did vertical climbing. This indicates that the ability of a gorilla to walk bipedally is not restricted by musculoskeletal adaptations for quadrupedalism and vertical climbing, at least in terms of moment arms and torque about hind limb joints.

Downsizing a giant: re-evaluating Dreadnoughtus body mass.

Estimates of body mass often represent the founding assumption on which biomechanical and macroevolutionary hypotheses are based. Recently, a scaling equation was applied to a newly discovered titanosaurian sauropod dinosaur (Dreadnoughtus), yielding a 59 300 kg body mass estimate for this animal. Herein, we use a modelling approach to examine the plausibility of this mass estimate for Dreadnoughtus. We find that 59 300 kg for Dreadnoughtus is highly implausible and demonstrate that masses above 40 000 kg require high body densities and expansions of soft tissue volume outside the skeleton several times greater than found in living quadrupedal mammals. Similar results from a small sample of other archosaurs suggests that lower-end mass estimates derived from scaling equations are most plausible for Dreadnoughtus, based on existing volumetric and density data from extant animals. Although volumetric models appear to more tightly constrain dinosaur body mass, there remains a clear need to further support these models with more exhaustive data from living animals. The relative and absolute discrepancies in mass predictions between volumetric models and scaling equations also indicate a need to systematically compare predictions across a wide size and taxonomic range to better inform studies of dinosaur body size.

Evaluation of a cadaveric wrist motion simulator using marker-based X-ray reconstruction of moving morphology.

Surgical intervention is a common option for the treatment of wrist joint arthritis and traumatic wrist injury. Whether this surgery is arthrodesis or a motion preserving procedure such as arthroplasty, wrist joint biomechanics are inevitably altered. To evaluate effects of surgery on parameters such as range of motion, efficiency and carpal kinematics, repeatable and controlled motion of cadaveric specimens is required. This study describes the development of a device that enables cadaveric wrist motion to be simulated before and after motion preserving surgery in a highly controlled manner. The simulator achieves joint motion through the application of predetermined displacements to the five major tendons of the wrist, and records tendon forces. A pilot experiment using six wrists aimed to evaluate its accuracy and reproducibility. Biplanar X-ray videoradiography (BPVR) and X-Ray Reconstruction of Moving Morphology (XROMM) were used to measure overall wrist angles before and after total wrist arthroplasty. The simulator was able to produce flexion, extension, radioulnar deviation, dart thrower's motion and circumduction within previously reported functional ranges of motion. Pre- and post-surgical wrist angles did not significantly differ. Intra-specimen motion trials were repeatable; root mean square errors between individual trials and average wrist angle and tendon force profiles were below 1° and 2 N respectively. Inter-specimen variation was higher, likely due to anatomical variation and lack of wrist position feedback. In conclusion, combining repeatable intra-specimen cadaveric motion simulation with BPVR and XROMM can be used to determine potential effects of motion preserving surgeries on wrist range of motion and biomechanics.

Regional variation of the cortical and trabecular bone material properties in the rabbit skull.

The material properties of some bones are known to vary with anatomical location, orientation and position within the bone (e.g., cortical and trabecular bone). Details of the heterogeneity and anisotropy of bone is an important consideration for biomechanical studies that apply techniques such as finite element analysis, as the outcomes will be influenced by the choice of material properties used. Datasets detailing the regional variation of material properties in the bones of the skull are sparse, leaving many finite element analyses of skulls no choice but to employ homogeneous, isotropic material properties, often using data from a different species to the one under investigation. Due to the growing significance of investigating the cranial biomechanics of the rabbit in basic science and clinical research, this study used nanoindentation to measure the elastic modulus of cortical and trabecular bone throughout the skull. The elastic moduli of cortical bone measured in the mediolateral and ventrodorsal direction were found to decrease posteriorly through the skull, while it was evenly distributed when measured in the anteroposterior direction. Furthermore, statistical tests showed that the variation of elastic moduli between separate regions (anterior, middle and posterior) of the skull were significantly different in cortical bone, but was not in trabecular bone. Elastic moduli measured in different orthotropic planes were also significantly different, with the moduli measured in the mediolateral direction consistently lower than that measured in either the anteroposterior or ventrodorsal direction. These findings demonstrate the significance of regional and directional variation in cortical bone elastic modulus, and therefore material properties in finite element models of the skull, particularly those of the rabbit, should consider the heterogeneous and orthotropic properties of skull bone when possible.

The evolution of compliance in the human lateral mid-foot.

Fossil evidence for longitudinal arches in the foot is frequently used to constrain the origins of terrestrial bipedality in human ancestors. This approach rests on the prevailing concept that human feet are unique in functioning with a relatively stiff lateral mid-foot, lacking the significant flexion and high plantar pressures present in non-human apes. This paradigm has stood for more than 70 years but has yet to be tested objectively with quantitative data. Herein, we show that plantar pressure records with elevated lateral mid-foot pressures occur frequently in healthy, habitually shod humans, with magnitudes in some individuals approaching absolute maxima across the foot. Furthermore, the same astonishing pressure range is present in bonobos and the orangutan (the most arboreal great ape), yielding overlap with human pressures. Thus, while the mean tendency of habitual mechanics of the mid-foot in healthy humans is indeed consistent with the traditional concept of the lateral mid-foot as a relatively rigid or stabilized structure, it is clear that lateral arch stabilization in humans is not obligate and is often transient. These findings suggest a level of detachment between foot stiffness during gait and osteological structure, hence fossilized bone morphology by itself may only provide a crude indication of mid-foot function in extinct hominins. Evidence for thick plantar tissues in Ardipithecus ramidus suggests that a human-like combination of active and passive modulation of foot compliance by soft tissues extends back into an arboreal context, supporting an arboreal origin of hominin bipedalism in compressive orthogrady. We propose that the musculoskeletal conformation of the modern human mid-foot evolved under selection for a functionally tuneable, rather than obligatory stiff structure.

The Functional and Anatomical Impacts of Healthy Muscle Ageing.

Even "healthy" muscle ageing is often associated with substantial changes in muscle form and function and can lead to increased injury risks and significant negative impacts on quality of life. However, the impacts of healthy muscle ageing on the fibre architecture and microstructure of different muscles and muscle groups throughout the lower limb, and how these are related to their functional capabilities, are not fully understood. Here, a previously established framework of magnetic resonance and diffusion tensor imaging was used to measure the muscle volumes, intramuscular fat, fibre lengths and physiological cross-sectional areas of 12 lower limb muscles in a cohort of healthily aged individuals, which were compared to the same data from a young population. Maximum muscle forces were also measured from an isokinetic dynamometer. The more substantial interpopulation differences in architecture and functional performance were located within the knee extensor muscles, while the aged muscles were also more heterogeneous in muscle fibre type and atrophy. The relationships between architecture and muscle strength were also more significant in the knee extensors compared to other functional groups. These data highlight the importance of the knee extensors as a potential focus for interventions to negate the impacts of muscle ageing.