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

Abstract

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.

From Fairies to Giants: Untangling the Effect of Body Size, Phylogeny, and Ecology on Vertebral Bone Microstructure of Xenarthran Mammals

“…The only metric with a significant correlation with body size for sloths is CSA, and most metrics have R -squared less than 0.05 ( Table 3 ). It is unclear whether this is due to the small body size range or the suspensory ecology of extant sloths, which results in unique loading of the vertebral column in sloths ( Nyakatura and Fischer 2010 ; Olson et al 2018 ; Alfieri et al 2021 ).…”

“…The impressive diversity of extinct sloths could greatly increase the range of sizes and ecologies represented in the clade, allowing us to better examine the relationship between TBA, body size, and ecology within this group. There has been some examination of extinct sloth TBA, but not enough to provide any insight into how scaling or ecology impact the TBA of their vertebrae; these papers did not include sufficient data to use in our analyses ( Fariña and Blanco 1996 ; Per Christiansen and Fariña 2003 ; Brandoni et al 2010 ; Amson et al 2015 ; Montañez-Rivera et al 2018 ; Alfieri et al 2021 ). In particular, it would provide an excellent test of whether the unusual TBA properties of extant sloths is a characteristic of all folivorans, or one that stems from a suspensory lifestyle ( Amson et al 2017 ; Montañez-Rivera et al 2018 ; Alfieri et al 2021 ).…”

“…Parsing the influence of body size, ecology, and phylogeny on trabecular bone is complicated. However, the effect of body size on TBA has been previously examined in birds, reptiles, mammals, rodents, primates, and humans, and many aspects of TBA scale allometrically ( Swartz et al 1998 ; Doube et al 2011 ; Barak et al 2013 ; Fajardo et al 2013 ; Ryan and Shaw 2013 ; Mielke et al 2018 ; Wysocki and Tseng 2018 ; Plasse et al 2019 ; Saers et al 2019 ; Alfieri et al 2021 ; Amson and Bibi 2021 ). Trabeculae have a minimum thickness of about 50 µm and a maximum of 460 µm, resulting from the mechanical limitations of osteoclasts and osteocytes, respectively ( Lozupone and Favia 1990 ; Mullender and Huiskes 1995 ; Barak et al 2013 ; Ryan and Shaw 2013 ), and trabecular thickness (Tb.Th) scales with negative allometry with body size ( Barak et al 2013 ; Ryan and Shaw 2013 ).…”

“…Scaling in the trabecular bone of xenarthrans has rarely been examined previously, but the superorder offers a phylogenetically conserved and ecologically diverse group of mammals in which to examine the impact of body size, ecology, and phylogeny on TBA ( Fig. 1 ) ( Amson et al 2017 ; Alfieri et al 2021 ). Modern xenarthrans provide an opportunity to examine the details of scaling patterns across a more limited size range and phylogenetic scale than in mammal-wide datasets.…”

Convergent Genomic Signatures of High-Altitude Adaptation among Six Independently Evolved Mammals

“…Not only could the same diet habits lead to the convergent evolution of different species, but also the same living habits could lead to the eco-morphological convergence of different species. Previous studies found that there was eco-morphological convergence in slow arboreal xenarthrans through the analysis of multiple omics of the humeral and femoral internal structure [ 15 ]. Independently evolving species might lead to the convergent evolution of phenotypes in order to adapt to the same environment, but these convergent phenotypes do not necessarily result from convergent evolution at the molecular level.…”