Vertical clinging and leaping induced evolutionary rate shifts in postcranial evolution of tamarins and marmosets (Primates, Callitrichidae)

Background: Callitrichids comprise a diverse group of platyrrhine monkeys that are present across South and Central America. Their secondarily evolved small size and pointed claws allow them to cling to vertical trunks of a large diameter. Within callitrichids, lineages with a high affinity for vertical supports often engage in trunk-to-trunk leaping. This vertical clinging and leaping (VCL) differs from horizontal leaping (HL) in terms of the functional demands imposed on the musculoskeletal system, all the more so as HL often occurs on small compliant terminal branches. We used quantified shape descriptors (3D geometric morphometrics) and phylogenetically-informed analyses to investigate the evolution of the shape and size of the humerus and femur, and how this variation reflects locomotor behavior within Callitrichidae. Results: The humerus of VCL-associated species has a narrower trochlea compared with HL species. It is hypothesized that this contributes to greater elbow mobility. The wider trochlea in HL species appears to correspondingly provide greater stability to the elbow joint. The femur in VCL species has a smaller head and laterally-oriented distal condyles, possibly to reduce stresses during clinging. Similarly, the expanded lesser trochanters visible in VCL species provide a greater lever for the leg retractors and are thus also interpreted as an adaptation to clinging. Evolutionary rate shifts to faster shape and size changes of humerus and femur occurred in the Leontocebus clade when a shift to slower rates occurred in the Saguinus clade. Conclusions: Based on the study of evolutionary rate shifts, the transition to VCL behavior within callitrichids (specifically the Leontocebus clade) appears to have been an opportunity for radiation, rather than a specialization that imposed constraints on morphological diversity. The study of the evolution of callitrichids suffers from a lack of comparative analyses of limb mechanics during trunk-to-trunk leaping, and future work in this direction would be of great interest.Peer Reviewe

Tools for quantitative form description : an evaluation of different software packages for semi-landmark analysis

The challenging complexity of biological structures has led to the development of several methods for quantitative analyses of form. Bones are shaped by the interaction of historical (phylogenetic), structural, and functional constrains. Consequently, bone shape has been investigated intensively in an evolutionary context. Geometric morphometric approaches allow the description of the shape of an object in all of its biological complexity. However, when biological objects present only few anatomical landmarks, sliding semi-landmarks may provide good descriptors of shape. The sliding procedure, mandatory for sliding semi-landmarks, requires several steps that may be time-consuming. We here compare the time required by two different software packages ('Edgewarp' and 'Morpho') for the same sliding task, and investigate potential differences in the results and biological interpretation. 'Morpho' is much faster than 'Edgewarp,' notably as a result of the greater computational power of the 'Morpho' software routines and the complexity of the 'Edgewarp' workflow. Morphospaces obtained using both software packages are similar and provide a consistent description of the biological variability. The principal differences between the two software packages are observed in areas characterized by abrupt changes in the bone topography. In summary, both software packages perform equally well in terms of the description of biological structures, yet differ in the simplicity of the workflow and time needed to performthe analyses

Integrative Approach Uncovers New Patterns of Ecomorphological Convergence in Slow Arboreal Xenarthrans

Identifying ecomorphological convergence examples is a central focus in evolutionary biology. In xenarthrans, slow arboreality independently arose at least three times, in the two genera of ‘tree sloths’, Bradypus and Choloepus, and the silky anteater, Cyclopes. This specialized locomotor ecology is expectedly reflected by distinctive morpho-functional convergences. Cyclopes, although sharing several ecological features with ‘tree sloths’, do not fully mirror the latter in their outstandingly similar suspensory slow arboreal locomotion. We hypothesized that the morphology of Cyclopes is closer to ‘tree sloths’ than to anteaters, but yet distinct, entailing that slow arboreal xenarthrans evolved through ‘incomplete’ convergence. In a multivariate trait space, slow arboreal xenarthrans are hence expected to depart from their sister taxa evolving toward the same area, but not showing extensive phenotypical overlap, due to the distinct position of Cyclopes. Conversely, a pattern of ‘complete’ convergence (i.e., widely overlapping morphologies) is hypothesized for ‘tree sloths’. Through phylogenetic comparative methods, we quantified humeral and femoral convergence in slow arboreal xenarthrans, including a sample of extant and extinct non-slow arboreal xenarthrans. Through 3D geometric morphometrics, cross-sectional properties (CSP) and trabecular architecture, we integratively quantified external shape, diaphyseal anatomy and internal epiphyseal structure. Several traits converged in slow arboreal xenarthrans, especially those pertaining to CSP. Phylomorphospaces and quantitative convergence analyses substantiated the expected patterns of ‘incomplete’ and ‘complete’ convergence for slow arboreal xenarthrans and ‘tree sloths’, respectively. This work, highlighting previously unidentified convergence patterns, emphasizes the value of an integrative multi-pronged quantitative approach to cope with complex mechanisms underlying ecomorphological convergence.Humboldt-Universität zu Berlin (1034)Peer Reviewe

adaptation across biologically relevant ‘levels’ in tamarins

The article processing charge was funded by the Open Access Publication Fund of Humboldt-Universität zu Berlin.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.Peer Reviewe

From land to water: evolutionary changes in long bone microanatomy of otters (Mammalia: Mustelidae)

International audienceAdaptation to an aquatic lifestyle has occurred independently in numerous amniote lineages. Such ecological shifts commonly engender adaptive changes in the musculoskeletal system. Semi-aquatic taxa highlight the compromises needed to enable locomotion both on land and in water and during the initial stages of the transition from land to water. Interestingly, mustelids include some semi-aquatic taxa that are primarily terrestrial and others that are primarily aquatic. Using microtomography, the inner bone structure of the whole stylopod from eight different mustelid taxa with distinct swimming abilities and ecologies was submitted to qualitative and quantitative analysis. Three main patterns in the three-dimensional inner organization of bone were identified, which illustrate three steps in the process of secondary adaptation to an aquatic lifestyle. These include a tubular organization in (primarily) terrestrial forms, a thickening of the cortex and an extension of the trabecular network in most otters, and a strong thickening of the cortex and a much denser and more widespread trabecular network in the almost exclusively aquatic sea otter. Microanatomical data are in agreement with morphological data and highlight consistency between the forearm and hindlimb patterns. The osteosclerotic pattern of the sea otter shows similarities to those of some aquatic amni-otes, but additional comparative three-dimensional microanatomical data are required to elucidate its functional significance. ADDITIONAL KEYWORDS: bone mass increase-long bones-microanatomy-Mustelidae-osteosclerosis-semi-aquatic

Swimmers, Diggers, Climbers and More, a Study of Integration Across the Mustelids' Locomotor Apparatus (Carnivora: Mustelidae)

International audiencePhenotypic integration, defined as the coordinated co-variation of parts of an organism can be an important constraint on phenotypic diversification. Functional factors, by having an heterogeneous impact across the animal body, may reinforce the integration of some parts while causing a perturbation of the integration among other parts. The integration across the locomotor apparatus should thus reflect to a certain extent the locomotor ecology of the animal. Using the mustelids as study group, we track changes in the patterns of co-variation in species belonging to four different locomotor ecologies (terrestrial, semi-arboreal, semi-fossorial, and semi-aquatic). Our results highlight the strong overall integration in mustelid long bones. The main shape changes associated with co-variations between skeletal elements are the bone robustness and proportions of the epiphyses. The pattern of co-variation is, however, only slightly impacted by allometry. Changes in co-variation between species mostly scale with phylogenetic divergence time, except for the (Mustela putorius, M. eversmanni, M. lutreola) clade which, despite a short divergence time, presents strong differences in co-variation. Co-variation patterns differ between locomotor ecologies, but few of these variations match the hypothesis of a reduction of integration due to functional specialization. This may reflect our lack of knowledge on the functional modules in species with locomotor ecologies that differ from terrestrial locomotion rather than invalidate our a priori hypotheses

Swimming and running: a study of the convergence in long bone morphology among semi-aquatic mustelids (Carnivora: Mustelidae)

International audienc

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

Abstract 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

Swimmers, Diggers, Climbers and More, a Study of Integration Across the Mustelids’ Locomotor Apparatus (Carnivora: Mustelidae)

International audienc