Evolution of bone cortical compactness in slow arboreal mammals

Abstract

Convergent evolution is a major topic in evolutionary biology. Low bone cortical compactness (CC, a measure of porosity of cortical bone) in the extant genera of “tree sloths,” has been linked to their convergent slow arboreal ecology. This proposed relationship of low CC with a slow arboreal lifestyle suggests potential convergent evolution of this trait in other slow arboreal mammals. Femoral and humeral CC were analyzed in “tree sloths,” lorisids, koala, and extinct palaeopropithecids and Megaladapis, in comparison to closely related but ecologically distinct taxa, in a phylogenetic framework. Low CC in “tree sloths” is unparalleled by any analyzed clade and the high CC in extinct sloths suggests the recent convergence of low CC in “tree sloths.” A tendency for low CC was found in Palaeopropithecus and Megaladapis. However, lorisids and the koala yielded unexpected CC patterns, preventing the recognition of a straightforward convergence of low CC in slow arboreal mammals. This study uncovers a complex relationship between CC and convergent evolution of slow arboreality, highlighting the multifactorial specificity of bone microstructure.

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

“…However, the locomotion of the silky anteater may also be categorized as antipronograde (sensu Granatosky et al 2014), in that forelimbs and/or hindlimbs are mainly loaded in tension, a feature shared by suspensory and vertical climbers (Preuschoft 2002;Nyakatura and Andrada 2013;Schmitt 2017, 2019;Hanna et al 2017). Several traits of this species have previously been identified as possible adaptations to fully arboreal vertical climbing (White 1993;Fonseca et al 1996;Nowak 1999), some of which are shared with Choloepus and Bradypus (White 1993;Lewton and Dingwall 2016;Alfieri et al 2021;Toledo et al 2021). Hereafter, we will consider 'tree sloths' and the silky anteater as slow arboreal species, meaning that this type of locomotion evolved three times independently in xenarthrans (Fig.…”

“…Despite implying phenotypic predictability from ecology (Losos et al 1998;Collar et al 2014), convergence may not manifest with the expected patterns and magnitude. Analyses of ecomorphological convergence yielded only partial confirmation for functional traits expected to be shared by mammals occupying the same ecological niche (e.g., Meloro et al 2015;Grossnickle et al 2020;Alfieri et al 2021). Several factors may be behind these outcomes, such as historical contingency/constraints (Harvey and Pagel 1991;Losos and Miles 1994;Zelditch et al 2017) or stochastic evolution (Stayton 2008(Stayton , 2015b.…”

“…Indeed, although extinct Folivora are characterized by an astonishing ecological diversity, no fossils have provided evidence of slow arboreality (McKenna and Bell 1997;Pujos et al 2007Pujos et al , 2017Gaudin and McDonald 2008). The distinct locomotor ecology of 'tree sloths' and its constraints drove the common acquisition of numerous traits (Nyakatura and Fischer 2011;Nyakatura 2012;Amson and Nyakatura 2018b;Montañez-Rivera et al 2018;de Oliveira and Santos 2018;Serio et al 2020;Alfieri et al 2021;Toledo et al 2021).…”

“…Moreover, previous analyses on Cyclopes have mainly been focused on locomotor habits shared with other anteaters (e.g., Amson et al 2017). Nevertheless, several ecological/biomechanical adaptations are present in both 'tree sloths' and Cyclopes, which can justify ascribing them to a slow arboreal ecology (following Alfieri et al 2021). Bradypus, Choloepus, and Cyclopes are overall characterized by cautious movements on trees, dominance of rest and quiescence in their daily activity balance, and extremely low basal metabolic rates (van Tyne 1929;Hayssen et al 2012;Nagy and Montgomery 2012;Nyakatura 2012;Pauli et al 2016;Vendl et al 2016).…”

“…Several traits are shared by the humeri and femora of slow arboreal xenarthrans (e.g., White 1993;Straehl et al 2013;Toledo et al 2013Toledo et al , 2015Amson and Nyakatura 2018b;de Oliveira and Santos 2018;Marshall et al 2021) including features related to the anatomical scales and/or techniques employed in this work. Indeed, humeral and/or femoral features shared by slow arboreal xenarthrans have been highlighted analysing the external 3D shape (Milne and O'Higgins 2012;Mielke et al 2018a), the diaphyseal structure (Patel et al 2013;Marchi et al 2016;Amson and Nyakatura 2018a;Montañez-Rivera et al 2018;Alfieri et al 2021) Fig. 2 Humerus of Choloepus didactylus NMW B5971 (left) and femur of Bradypus tridactylus ZMB Mam 7614 (right).…”