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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)

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.

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