Linking morphology, performance, and habitat utilization: adaptation across biologically relevant 'levels' in tamarins.

BACKGROUND: Biological adaptation manifests itself at the interface of different biologically relevant 'levels', such as ecology, performance, and morphology. Integrated studies at this interface are scarce due to practical difficulties in study design. We present a multilevel analysis, in which we combine evidence from habitat utilization, leaping performance and limb bone morphology of four species of tamarins to elucidate correlations between these 'levels'. RESULTS: We conducted studies of leaping behavior in the field and in a naturalistic park and found significant differences in support use and leaping performance. Leontocebus nigrifrons leaps primarily on vertical, inflexible supports, with vertical body postures, and covers greater leaping distances on average. In contrast, Saguinus midas and S. imperator use vertical and horizontal supports for leaping with a relatively similar frequency. S. mystax is similar to S. midas and S. imperator in the use of supports, but covers greater leaping distances on average, which are nevertheless shorter than those of L. nigrifrons. We assumed these differences to be reflected in the locomotor morphology, too, and compared various morphological features of the long bones of the limbs. According to our performance and habitat utilization data, we expected the long bone morphology of L. nigrifrons to reflect the largest potential for joint torque generation and stress resistance, because we assume longer leaps on vertical supports to exert larger forces on the bones. For S. mystax, based on our performance data, we expected the potential for torque generation to be intermediate between L. nigrifrons and the other two Saguinus species. Surprisingly, we found S. midas and S. imperator having relatively more robust morphological structures as well as relatively larger muscle in-levers, and thus appearing better adapted to the stresses involved in leaping than the other two. CONCLUSION: This study demonstrates the complex ways in which behavioral and morphological 'levels' map onto each other, cautioning against oversimplification of ecological profiles when using large interspecific eco-morphological studies to make adaptive evolutionary inferences.

A macroevolutionary common-garden experiment reveals differentially evolvable bone organization levels in slow arboreal mammals.

Eco-morphological convergence, i.e., similar phenotypes evolved in ecologically convergent taxa, naturally reproduces a common-garden experiment since it allows researchers to keep ecological factors constant, studying intrinsic evolutionary drivers. The latter may result in differential evolvability that, among individual anatomical parts, causes mosaic evolution. Reconstructing the evolutionary morphology of the humerus and femur of slow arboreal mammals, we addressed mosaicism at different bone anatomical spatial scales. We compared convergence strength, using it as indicator of evolvability, between bone external shape and inner structure, with the former expected to be less evolvable and less involved in convergent evolution, due to anatomical constraints. We identify several convergent inner structural traits, while external shape only loosely follows this trend, and we find confirmation for our assumption in measures of convergence magnitude. We suggest that future macroevolutionary reconstructions based on bone morphology should include structural traits to better detect ecological effects on vertebrate diversification.

Evolution of gliding in squirrel-related rodents (Mammalia: Sciuromorpha) did not induce a new optimum on the cortical thickness of the scapular glenoid fossa.

Many of the squirrel-related rodents (i.e., Sciuromorpha) are tree-dwelling species known to be very agile climbers. This taxon also includes the most diverse clade of gliding (aerial) mammals that likely descended from a non-gliding arboreal ancestor and evolved a patagium (i.e., a gliding membrane) to increase gliding performance. Glides can cover distances of up to 150 m and landing is typically accomplished by stalling the patagium to reduce impact velocity. It remains unclear if this behavior suffices to keep stresses on the locomotor apparatus similar to those experienced by their arboreal relatives or whether gliding behavior increases landing forces and stresses. The sparsely available support reaction force data are ambiguous, but bone microstructure is highly adaptable to changes in loading regime and likely provides insights into this question. Using µCT scans, we compared the cortical thickness of the glenoid fossa of the shoulder joint between arboreal and aerial Sciuromorpha using evolutionary model comparison, while also accounting for regional differences of the glenoid fossa. We did not find any differences between these locomotor behaviors, irrespective of the glenoid region. These findings agree with previous analyses of the microstructure of the femur in Sciuromorpha. We discuss different aspects that could explain the similarity in cortical thickness. According to our analysis of glenoid cortical thickness the loading regime appears not to have changed after the evolution of gliding locomotion, likely due to adjustments in landing performance.

Groovy and Gnarly: Surface Wrinkles as a Multifunctional Motif for Terrestrial and Marine Environments.

From large ventral pleats of humpback whales to nanoscale ridges on flower petals, wrinkled structures are omnipresent, multifunctional, and found at hugely diverse scales. Depending on the particulars of the biological system-its environment, morphology, and mechanical properties-wrinkles may control adhesion, friction, wetting, or drag; promote interfacial exchange; act as flow channels; or contribute to stretching, mechanical integrity, or structural color. Undulations on natural surfaces primarily arise from stress-induced instabilities of surface layers (e.g., buckling) during growth or aging. Variation in the material properties of surface layers and in the magnitude and orientation of intrinsic stresses during growth lead to a variety of wrinkling morphologies and patterns which, in turn, reflect the wide range of biophysical challenges wrinkled surfaces can solve. Therefore, investigating how surface wrinkles vary and are implemented across biological systems is key to understanding their structure-function relationships. In this work, we synthesize the literature in a metadata analysis of surface wrinkling in various terrestrial and marine organisms to review important morphological parameters and classify functional aspects of surface wrinkles in relation to the size and ecology of organisms. Building on our previous and current experimental studies, we explore case studies on nano/micro-scale wrinkles in biofilms, plant surfaces, and basking shark filter structures to compare developmental and structure-vs-function aspects of wrinkles with vastly different size scales and environmental demands. In doing this and by contrasting wrinkle development in soft and hard biological systems, we provide a template of structure-function relationships of biological surface wrinkles and an outlook for functionalized wrinkled biomimetic surfaces.

Computational Modeling of Gluteus Medius Muscle Moment Arm in Caviomorph Rodents Reveals Ecomorphological Specializations.

Vertebrate musculoskeletal locomotion is realized through lever-arm systems. The instantaneous muscle moment arm (IMMA), which is expected to be under selective pressure and thus of interest for ecomorphological studies, is a key aspect of these systems. The IMMA changes with joint motion. It's length change is technically difficult to acquire and has not been compared in a larger phylogenetic ecomorphological framework, yet. Usually, proxies such as osteological in-levers are used instead. We used 18 species of the ecologically diverse clade of caviomorph rodents to test whether its diversity is reflected in the IMMA of the hip extensor M. gluteus medius. A large IMMA is beneficial for torque generation; a small IMMA facilitates fast joint excursion. We expected large IMMAs in scansorial species, small IMMAs in fossorial species, and somewhat intermediate IMMAs in cursorial species, depending on the relative importance of acceleration and joint angular velocity. We modeled the IMMA over the entire range of possible hip extensions and applied macroevolutionary model comparison to selected joint poses. We also obtained the osteological in-lever of the M. gluteus medius to compare it to the IMMA. At little hip extension, the IMMA was largest on average in scansorial species, while the other two lifestyles were similar. We interpret this as an emphasized need for increased hip joint torque when climbing on inclines, especially in a crouched posture. Cursorial species might benefit from fast joint excursion, but their similarity with the fossorial species is difficult to interpret and could hint at ecological similarities. At larger extension angles, cursorial species displayed the second-largest IMMAs after scansorial species. The larger IMMA optimum results in powerful hip extension which coincides with forward acceleration at late stance beneficial for climbing, jumping, and escaping predators. This might be less relevant for a fossorial lifestyle. The results of the in-lever only matched the IMMA results of larger hip extension angles, suggesting that the modeling of the IMMA provides more nuanced insights into adaptations of musculoskeletal lever-arm systems than this osteological proxy.

Ontogeny of a tessellated surface: Carapace growth of the longhorn cowfish Lactoria cornuta.

Biological armors derive their mechanical integrity in part from their geometric architectures, often involving tessellations: individual structural elements tiled together to form surface shells. The carapace of boxfish, for example, is composed of mineralized polygonal plates, called scutes, arranged in a complex geometric pattern and nearly completely encasing the body. In contrast to artificial armors, the boxfish exoskeleton grows with the fish; the relationship between the tessellation and the gross structure of the armor is therefore critical to sustained protection throughout growth. To clarify whether or how the boxfish tessellation is maintained or altered with age, we quantify architectural aspects of the tessellated carapace of the longhorn cowfish Lactoria cornuta through ontogeny (across nearly an order of magnitude in standard length) and in a high-throughput fashion, using high-resolution microCT data and segmentation algorithms to characterize the hundreds of scutes that cover each individual. We show that carapace growth is canalized with little variability across individuals: rather than continually adding scutes to enlarge the carapace surface, the number of scutes is surprisingly constant, with scutes increasing in volume, thickness, and especially width with age. As cowfish and their scutes grow, scutes become comparatively thinner, with the scutes at the edges (weak points in a boxy architecture) being some of the thickest and most reinforced in younger animals and thinning most slowly across ontogeny. In contrast, smaller scutes with more variable curvature were found in the limited areas of more complex topology (e.g., around fin insertions, mouth, and anus). Measurements of Gaussian and mean curvature illustrate that cowfish are essentially tessellated boxes throughout life: predominantly zero curvature surfaces comprised of mostly flat scutes, and with scutes with sharp bends used sparingly to form box edges. Since growth of a curved, tiled surface with a fixed number of tiles would require tile restructuring to accommodate the surface's changing radius of curvature, our results therefore illustrate a previously unappreciated advantage of the odd boxfish morphology: by having predominantly flat surfaces, it is the box-like body form that in fact permits a relatively straightforward growth system of this tessellated architecture (i.e., where material is added to scute edges). Our characterization of the ontogeny and maintenance of the carapace tessellation provides insights into the potentially conflicting mechanical, geometric, and developmental constraints of this species but also perspectives into natural strategies for constructing mutable tiled architectures.

Weighing homoplasy against alternative scenarios with the help of macroevolutionary modeling: A case study on limb bones of fossorial sciuromorph rodents.

Homoplasy is a strong indicator of a phenotypic trait's adaptive significance when it can be linked to a similar function. We assessed homoplasy in functionally relevant scapular and femoral traits of Marmotini and Xerini, two sciuromorph rodent clades that independently acquired a fossorial lifestyle from an arboreal ancestor. We studied 125 species in the scapular dataset and 123 species in the femoral dataset. Pairwise evolutionary model comparison was used to evaluate whether homoplasy of trait optima is more likely than other plausible scenarios. The most likely trend of trait evolution among all traits was assessed via likelihood scoring of all considered models. The homoplasy hypothesis could never be confirmed as the single most likely model. Regarding likelihood scoring, scapular traits most frequently did not differ among Marmotini, Xerini, and arboreal species. For the majority of femoral traits, results indicate that Marmotini, but not Xerini, evolved away from the ancestral arboreal condition. We conclude on the basis of the scapular results that the forelimbs of fossorial and arboreal sciuromorphs share mostly similar functional demands, whereas the results on the femur indicate that the hind limb morphology is less constrained, perhaps depending on the specific fossorial habitat.

The evolution of femoral cross-sectional properties in sciuromorph rodents: Influence of body mass and locomotor ecology.

In several groups of mammals, adaptation to differing functional demands is reflected in long bone cross-sectional properties (CSP), which relate to the resistance to compression and to bending loads in the craniocaudal and mediolateral directions. Members of the Sciuromorpha ("squirrel-like" rodents) display a diversity of locomotor ecologies and span three orders of magnitude in terms of body size. The availability of robust phylogenies is rendering them a suitable group to further substantiate the relationship of long bone CSP with locomotor ecology and body mass while taking the phylogenetic non-independence among species into account. Here, we studied 69 species of Sciuromorpha belonging to three lifestyle categories, "arboreal," "fossorial," and "aerial" (i.e., gliding). We hypothesized locomotor category specific loading regimes that act on femora during predominant or, in terms of gliding, critical locomotor behaviors of each category. High resolution computed tomography scans of the specimens' femora were obtained and cross-sections in 5% increments were analyzed. Cross-sectional area, the craniocaudal second moment of area (SMAcc ), and the mediolateral second moment of area were quantified. Further, a scaling analysis was conducted for each bone cross-section to examine how the CSP scale with body mass. Body mass accounted for variances in CSP with mainly positive allometry. The aerial sciuromorphs showed lower values of CSP compared to the arboreal and fossorial species in the distal epiphysis for all quantified parameters and along the bone for SMAcc . In contrast to previous studies on other mammalian lineages, no differences in CSP were found between the fossorial and the arboreal lifestyles.

Femoral morphology of sciuromorph rodents in light of scaling and locomotor ecology.

Sciuromorph rodents are a monophyletic group comprising about 300 species with a body mass range spanning three orders of magnitude and various locomotor behaviors that we categorized into arboreal, fossorial and aerial. The purpose of this study was to investigate how the interplay of locomotor ecology and body mass affects the morphology of the sciuromorph locomotor apparatus. The most proximal skeletal element of the hind limb, i.e. the femur, was selected, because it was shown to reflect a functional signal in various mammalian taxa. We analyzed univariate traits (effective femoral length, various robustness variables and the in-levers of the muscles attaching to the greater, third and lesser trochanters) as well as femoral shape, representing a multivariate trait. An ordinary least-squares regression including 177 species was used to test for a significant interaction effect between body mass and locomotor ecology on the variables. Specifically, it tested whether the scaling patterns of the fossorial and aerial groups differ when compared with the arboreal, because the latter was identified as the ancestral sciuromorph condition via stochastic character mapping. We expected aerial species to display the highest trait values for a given body mass as well as the steepest slopes, followed by the arboreal and fossorial species along this order. An Ornstein-Uhlenbeck regression fitted to a phylogenetically pruned dataset of 140 species revealed the phylogenetic inertia to be very low in the univariate traits, hence justifying the utilization of standard regressions. These variables generally scaled close to isometry, suggesting that scaling adjustments might not have played a major role for most of the femoral features. Nevertheless, the low phylogenetic inertia indicates that the observed scaling patterns needed to be maintained during sciuromorph evolution. Significant interaction effects were discovered in the femoral length, the centroid size of the condyles, and the in-levers of the greater and third trochanters. Additionally, adjustments in various femoral traits reflect the acquisitions of fossorial and aerial behaviors from arboreal ancestors. Using sciuromorphs as a focal clade, our findings exemplify the importance of statistically accounting for potential interaction effects of different environmental factors in studies relating morphology to ecology.

Motion analysis of non-model organisms using a hierarchical model: Influence of setup enclosure dimensions on gait parameters of Swinhoe's striped squirrels as a test case.

In in-vivo motion analyses, data from a limited number of subjects and trials is used as proxy for locomotion properties of entire populations, yet the inherent hierarchy of the individual and population level is usually not accounted for. Despite the increasing availability of hierarchical model frameworks for statistical analyses, they have not been applied extensively to comparative motion analysis. As a case study for the use of hierarchical models, we analyzed locomotor parameters of four Swinhoe's striped squirrels. The small-bodied arboreal mammals exhibit brief bouts of rapid asymmetric gaits. Spatio-temporal parameters on runways with experimentally varied dimensions of the setup enclosure were compared to test for their potentially confounding effects. We applied principal component analysis to evaluate changes to the overall locomotor pattern. A common, non-hierarchical, pooled statistical analysis of the data revealed significant differences in some of the parameters depending on enclosure dimensions. In contrast, we used a hierarchical Bayesian generalized linear model (GLM) that considers subject specific differences and population effects to compare the effect of enclosure dimensions on the measured parameters and the principal components. None of the population effects were confirmed by the hierarchical GLM. The confounding effect of a single subject that deviates in its locomotor behavior is potentially bigger than the influence of the experimental variation in enclosure dimensions. Our findings justify the common practice of researchers to intuitively select an enclosure with dimensions assumed as "non-constraining". Hierarchical models can easily be designed to cope with limited sample size and bias introduced by deviating behavior of individuals. When limited data is available-a typical restriction of in-vivo motion analyses of non-model organisms-density distributions of the Bayesian GLM used here remain reliable and the hierarchical structure of the model optimally exploits all available information. We provide code to be adjusted to other research questions.

Trabecular architecture in the sciuromorph femoral head: allometry and functional adaptation.

BACKGROUND: Sciuromorpha (squirrels and close relatives) are diverse in terms of body size and locomotor behavior. Individual species are specialized to perform climbing, gliding or digging behavior, the latter being the result of multiple independent evolutionary acquisitions. Each lifestyle involves characteristic loading patterns acting on the bones of sciuromorphs. Trabecular bone, as part of the bone inner structure, adapts to such loading patterns. This network of thin bony struts is subject to bone modeling, and therefore reflects habitual loading throughout lifetime. The present study investigates the effect of body size and lifestyle on trabecular structure in Sciuromorpha. METHODS: Based upon high-resolution computed tomography scans, the femoral head 3D inner microstructure of 69 sciuromorph species was analyzed. Species were assigned to one of the following lifestyle categories: arboreal, aerial, fossorial and semifossorial. A cubic volume of interest was selected in the center of each femoral head and analyzed by extraction of various parameters that characterize trabecular architecture (degree of anisotropy, bone volume fraction, connectivity density, trabecular thickness, trabecular separation, bone surface density and main trabecular orientation). Our analysis included evaluation of the allometric signals and lifestyle-related adaptation in the trabecular parameters. RESULTS: We show that bone surface density, bone volume fraction, and connectivity density are subject to positive allometry, and degree of anisotropy, trabecular thickness, and trabecular separation to negative allometry. The parameters connectivity density, bone surface density, trabecular thickness, and trabecular separation show functional signals which are related to locomotor behavior. Aerial species are distinguished from fossorial ones by a higher trabecular thickness, lower connectivity density and lower bone surface density. Arboreal species are distinguished from semifossorial ones by a higher trabecular separation. CONCLUSION: This study on sciuromorph trabeculae supplements the few non-primate studies on lifestyle-related functional adaptation of trabecular bone. We show that the architecture of the femoral head trabeculae in Sciuromorpha correlates with body mass and locomotor habits. Our findings provide a new basis for experimental research focused on functional significance of bone inner microstructure.