Bone cortical compactness in ‘tree sloths’ reflects convergent evolution

Abstract

Bone remodeling, one of the main processes that regulate bone microstructure, consists of bone resorption followed by the deposition of secondary bone at the same location. Remodeling intensity varies among taxa, but a characteristically compact cortex is ubiquitous in the long bones of mature terrestrial mammals. A previous analysis found that cortical bone in a few 'tree sloth' (Bradypus and Choloepus) specimens is heavily remodeled and characterized by numerous immature secondary osteons, suggesting that these animals were remodeling their bones at high rate until late in their ontogeny. This study aims at testing if this remodeling is generally present in 'tree sloths', using a quantitative analysis of the humeral cortical compactness (CC) among xenarthrans. The results of the investigation of humeral diaphyseal cross-sections of 26 specimens belonging to 10 xenarthran species including specimens from both extinct and extant species indicate that in 'tree sloths' the CC is significantly lower than in the other sampled xenarthrans. No significant difference was found between the CC of the two genera of 'tree sloths'. Our results are consistent with the hypothesis that the cortical bone of 'tree sloths' in general undergoes intense and balanced remodeling that is maintained until late (possibly throughout) in their ontogeny. In the light of xenarthran phylogeny, low CC represents another convergence between the long-separated 'tree sloth' lineages. Although the exact structural and/or functional demands that are associated with this trait are hitherto unknown, several hypotheses are suggested here, including a relationship to their relatively low metabolism and to the mechanical demands imposed upon the bones by the suspensory posture and locomotion, which was independently acquired by the two genera of 'tree sloths'.

Palaeobiological inferences based on long bone epiphyseal and diaphyseal structure - the forelimb of xenarthrans (Mammalia)

“…The extremely low metabolism of extant sloths was suggested by Montañez-Rivera et al (2018) as a potential explaining factor for their low cortical compactness (CC). Indeed, they found that extant sloths depart in that regard from other extant xenarthrans as well as from two extinct sloths (the small-sized Hapalops and Parocnus).…”

Evolution of bone cortical compactness in slow arboreal mammals

“…The amount of porosities in the diaphyseal compact cortical bone, or cortical compactness (CC), was recently quantified in the humerus of adult extant and extinct xenarthrans. The two lineages of extant sloths ( Choloepus and Bradypus ), characterised by an exceptionally slow arboreal lifestyle [11], were found to feature lower CC in respect to other similar-sized taxa which conversely follow the generalised mammalian condition of high CC [12]. Because ‘tree sloths’ are not monophyletic (hence the quotation marks employed herein), this trait was identified as one of the convergent traits related to their independently acquired slow arboreal lifestyle [11,12].…”

“…This set of traits is generally associated with unusually low metabolic rate. To date, no CC analyses were performed on slow arboreal mammals, beside the one on ‘tree sloths’ [12]. Following the latter, we quantified CC in the humerus.…”

“…Noticeably, the sample characterised by distinct lifestyles includes specimens of extinct sloths from the Patagonian Early Miocene Santa Cruz Formation [22–24]. Analyzing them can additionally inform on the evolution of low CC in the two lineages of ‘tree sloths’ and corroborate the proposed recent convergence [12].…”

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

“…Homoplasy has been used as an indicator of the adaptive significance of these character states, especially when these can be associated with a similar function (Harvey & Pagel, ; Mayr, ; Nyakatura, ; Schluter, ; Simpson, ). Thus, it is not surprising that plenty of studies in functional morphology have been concerned with this phenomenon and aimed at unveiling particularly instructive cases of form–function relationships that evolved multiple times independently (e.g., Botton‐Divet, Cornette, Houssaye, Fabre, & Herrel, ; Dublin, ; Hildebrand & Goslow, ; Houssaye & Fish, ; Lull, ; Mahler, Ingram, Revell, & Losos, ; Moen, Irschick, & Wiens, ; Montañez‐Rivera, Nyakatura, & Amson, ; Muschick, Indermaur, & Salzburger, ; Osburn, ; Runestad & Ruff, ; Shimer, ).…”