The Convergent Evolution of Suspensory Posture and Locomotion in Tree Sloths

Abstract

Recent phylogenetic analyses imply a distant relationship and long separated evolution of two-toed sloths (Choloepus) and three-toed sloths (Bradypus). No known fossil sloth is interpreted to have been suspensory. As a consequence, the suspensory posture and locomotion of the extant genera likely evolved convergently in both lineages, forming a new framework for the analysis of functional aspects of the locomotor apparatus of extant tree sloths. The suspensory posture and locomotion has altered functional demands from the phylogenetically plesiomorphic nonsuspensory pronograde situation. Here, anatomical traits that have been argued to be of adaptive significance for quadrupedal suspensory locomotion are reviewed and the evolution of these traits is discussed in light of the new framework. Experimental data are largely limited to Choloepus, but help to deduce functional aspects of the anatomy in Bradypus as well. The most important adaptive traits are hands and feet modified into relatively rigid hooklike appendages, great mobility of all joints proximal to the midcarpal and transverse tarsal joints, relatively long arms with a relatively short scapula, a rounded thorax with a small diameter, a highly mobile sterno-clavicular articulation, and emphasis on powerful flexion in the proximal limb joints via advantageous lever arms. Despite these changes, patterns of limb kinematics remained conservative during the course of evolution in the lineages leading to extant tree sloths, and it is suggested here that this also applies to the pattern of neuromuscular control of limb movements during locomotion. Morphological 'solutions'to altered functional demands posed by inversed orientation of the body differ in the two genera of extant tree sloths, thereby corroborating the proposed diphyly. Convergent evolution in tree sloths may be attributed to functional constraints posed by fossorial adaptations in early Xenarthra that canalized sloths to adopt a suspensory posture and locomotion in the arboreal habitat.

Gait kinetics of above- and below-branch quadrupedal locomotion in lemurid primates

“…While numerous studies have focused on the mechanics of highly specialized forms of suspensory locomotion such as brachiation and arm swinging (Chang et al, 2000;Michilsens et al, 2010Michilsens et al, , 2011Swartz, 1989;Swartz et al, 1989;Turnquist et al, 1999), relatively few have explored the mechanics of below-branch quadrupedal locomotion (Ishida et al, 1990;Nyakatura, 2012;. Below-branch quadrupedal locomotion is a form of suspensory positional behavior that involves all four limbs, and superficially resembles the kinematics and timing of above-branch walking (Ishida et al, 1990;Jouffroy and Petter, 1990;Jouffroy and Stern, 1990;Parsons and Taylor, 1977).…”

“…sloths, bats, kinkajous), few studies (Fujiwara et al, 2011;Ishida et al, 1990;Jouffroy and Petter, 1990;Jouffroy and Stern, 1990;Mendel, 1981;Nyakatura, 2012;Parsons and Taylor, 1977;Turnquist, 1975) have specifically focused on the mechanics of below-branch quadrupedal locomotion in mammals, and of those only one has measured substrate reaction forces (Ishida et al, 1990). Ishida et al (1990) collected multiaxial force data from freely moving slow lorises (Nycticebus coucang) on an upright and inverted instrumented runway.…”

The Topographic Organization of Retinal Ganglion Cell Density and Spatial Resolving Power in an Unusual Arboreal and Slow-Moving Strepsirhine Primate, the Potto <b><i>(Perodicticus potto)</i></b>

“…As with sloths, pottos move on the lower surface of branches but also commonly use the upper surfaces and are able to rotate or spiral around the branches [Walker, 1969;Oates, 1984;Nekaris, 2013]. This maneuverability contrasts with the predominantly suspensory locomotion on the underside of branches of sloths [Miller, 1935;Nyakatura, 2012], and requires a 13 more three-dimensional visual sampling across different angles of the branches for which a more concentric organization of retinal ganglion cells is useful. Among primates, the presence of a well-developed fovea is a distinctive feature.…”

Genomic evidence for rod monochromacy in sloths and armadillos suggests early subterranean history for Xenarthra

“…The earliest xenarthran fossils (Middle Palaeocene) show fossorial limb adaptations [67] and extant armadillos and many extinct xenarthrans display(ed) fossorial behaviours and/or adaptations [68][69][70][71][72][73][74]. Though extant anteaters and sloths are terrestrial to arboreal, xenarthran synapomorphies include features that reflect a fossorial ancestry: strongly curved claws; a secondary scapular spine, allowing for a stronger retraction of the humerus [75]; plus a synsacrum and lateral accessory articulations of the lumbar vertebrae, which help stabilize the body while digging [76,77]. Besides xenarthrans, the latter character is present only in the subterranean Mesozoic mammal Fruitafossor [64].…”

“…gliding, flying, running) and feeding habits (e.g. active predation), and canalized tree sloths to convergently adopt a suspensory posture [77]. The presence of rod monochromacy in xenarthrans should be taken into account in future behavioural, ecological and conservation studies involving this enigmatic lineage of mammals.…”