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Vertical Support Use and Primate Origins Gabriel S www.nature.com/scientificreports OPEN Vertical support use and primate origins Gabriel S. Yapuncich 1, Henry J. Feng1, Rachel H. Dunn2, Erik R. Seifert 3 & Doug M. Boyer1 Adaptive scenarios of crown primate origins remain contentious due to uncertain order of acquisition Received: 1 May 2019 and functional signifcance of the clade’s diagnostic traits. A feature of the talus bone in the ankle, Accepted: 6 August 2019 known as the posterior trochlear shelf (PTS), is well-regarded as a derived crown primate trait, but Published: xx xx xxxx its adaptive signifcance has been obscured by poorly understood function. Here we propose a novel biomechanical function for the PTS and model the talus as a cam mechanism. By surveying a large sample of primates and their closest relatives, we demonstrate that the PTS is most strongly developed in extant taxa that habitually grasp vertical supports with strongly dorsifexed feet. Tali of the earliest fossils likely to represent crown primates exhibit more strongly developed PTS cam mechanisms than extant primates. As a cam, the PTS may increase grasping efciency in dorsifexed foot postures by increasing the path length of the fexor fbularis tendon, and thus improve the muscle’s ability to maintain fexed digits without increasing energetic demands. Comparisons are made to other passive digital fexion mechanisms suggested to exist in other vertebrates. These results provide robust anatomical evidence that the habitual vertical support use exerted a strong selective pressure during crown primate origins. Te talus is an important element for reconstructing positional behavior throughout primate evolution because the bone’s morphology correlates well with locomotor and postural behaviors of living euarchontans (the mam- malian clade including Primates, Scandentia, Dermoptera) and it is frequently preserved in fossil assemblages1–4. However, despite a long history of study1,4–7, debate remains concerning the talar morphology of the common ancestor of crown primates and the positional behavior implied by this morphology. Te posterior trochlear shelf (PTS) – a bony extension protruding from the posterior aspect of the talar body (Fig. 1) – is a prime example of a conspicuous but confounding talar feature: while PTS hypertrophy unequivocally diagnoses a crown primate talus1, there is no consensus regarding the feature’s functional signifcance2,7. Several biomechanical roles have been suggested, including creating a bony stop during plantarfexion1,2, supporting an elongated posterior cal- caneal facet1,4, or redirecting stress within the talus4. Te ambiguous function of the PTS means it is ofen char- acterized but rarely emphasized in the description of fossil tali3,7. Resolving this gap in understanding of primate functional anatomy can provide novel insights into the origin of our order. From a biomechanical perspective, PTS hypertrophy accentuates an asymmetry around the axis of the talocru- ral joint. As a hinge joint, the talocrural joint is primarily involved in dorsi- and plantarfexion of the foot as the talus rotates sagittally around a largely transverse axis8 (although more complex movements in other anatomi- cal planes occur at the joint as well9,10). A rotating, asymmetrical body can function as a cam mechanism (Fig. S1a), converting rotational into translational motion11. Cams consist of two moving elements: a driver, which is generally fxed at a rotational axis and has an asymmetry known as the rise, and a follower, which contacts the driver and follows a path dictated by the contour of the rise (Fig. S1a). We hypothesize that the talus functions as a driver rotating about the talocrural joint axis, the PTS serves as the rise, and the tendon of the fexor fbularis muscle (transmitted through a groove on the posterior aspect of the talus) as the follower. Rotation of the driver (dorsi- and plantarfexion of the foot) would “translate” the tendon proximally by increasing its path length, and a larger rise (i.e., PTS hypertrophy) would increase the efect. Since the PTS is located on the posterior aspect of the talus, the tendon’s path length would be maximized when the PTS is most distal to the origin of the fexor fbularis (i.e., when the foot is dorsifexed) and the tendon would be “translated” toward the muscle’s origin, efectively contracting the muscle (Fig. 2). 1Department of Evolutionary Anthropology, Duke University, Durham, NC, 27708, USA. 2Department of Anatomy, Des Moines University, Des Moines, IA, 50312, USA. 3Department of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, 90033, USA. Correspondence and requests for materials should be addressed to G.S.Y. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:12341 | https://doi.org/10.1038/s41598-019-48651-x 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. Presence and absence of the posterior trochlear shelf (PTS) in euarchontans. PTS indicated by shading. Ellipses represent fexor fbularis tendon; tendons in red are expected to experience cam efect, while tendons in blue are not. Non-crown primates include (a) Ptilocercus lowii (USNM 488072), (b) Galeopterus variegatus (USNM 317118), and (c) †Plesiadapis rex (UM 94816; reversed for consistency). Extant and likely crown primates include (d) †Teilhardina belgica (IRSNB M1235), (e) †Donrussellia provincialis (MNHN RI 428), and (f) Lepilemur mustelinus (AMNH 170556). Institution abbreviations and expanded comparative plates are provided in Supplementary Material. Scale bars equal 3 mm. In non-human primates, the fexor fbularis typically inserts on the distal phalanges of the frst, third, and fourth rays12, so the PTS cam mechanism could confer several biomechanical benefts in taxa with grasping feet. Given the muscle’s insertion patterns and assuming muscular contraction remains constant, translation of the tendon may induce additional fexion of digits critical for pedal grasping (Fig. 2). Alternatively, increasing the path length of the tendon during dorsifexion could permit reduced muscular activity without a concomitant decrease in grasping ability. Finally, the PTS cam could increase the passive tension within the muscle: when stretched to a certain length, the actin-myosin interaction of sarcomeres is maximized, permitting increased force generation13. If the fexor fbularis can stretch the additional distance necessitated by a hypertrophied PTS, the cam mechanism could shif the muscle to a more efcient position along its length-tension curve. In the discussion, we examine the likelihood of each of these alternatives, but in all cases, a hypertrophied PTS would increase grasping efciency (increased work for equivalent energy or equivalent work for reduced energy) in a dorsifexed foot posture. To model the PTS as a cam mechanism, our measurements capture the size of the rise relative to the base circle of the driver, a ratio termed the PTS index (Fig. S1b). PTS indices > 1 indicate strongly developed cam mecha- nisms (Materials and Methods). We compute PTS indices for a large and comprehensive sample of euarchontans (Materials and Methods) and test for signifcant diferences between clades as well as signifcant diferences from a PTS index = 1 (a null hypothesis indicating the rise is equivalent to the driver’s base circle). Finally, we eval- uate the evolution of the PTS through time using Bayesian ancestral state reconstruction and multiple-regime Ornstein-Uhlenbeck models (Materials and Methods). Results Among extant primates, the highest PTS indices are exhibited by indriids and Lepilemur (Fig. 3a; Table S1; Fig. S6). Four extant primate families (Indriidae, Lemuridae, Galagidae, and Tarsiidae), as well as a non-natural group of the remaining lemuriform taxa (Cheirogaleidae, Lepilemur, and Daubentonia) have mean PTS indices signif- cantly greater than 1 (Table S8). Of these taxa, indriids, galagids, and tarsiers habitually grasp vertically oriented supports with strongly dorsifexed feet14–16, and vertical support use is a component of the positional behavior for many lemuriforms17. As a group, strepsirrhines (excluding Lorisidae) have signifcantly greater PTS indices than anthropoids, lorisids, and other euarchontans (dermopterans and scandentians) (Fig. 3a; Table S7; Fig. S5). Te high PTS indices of extant vertical clinging taxa are exceeded by those of several fossil groups. Members of both adapiforms and omomyiforms, two Eocene groups likely to represent crown primates, including the earliest represented members (Donrussellia and Teilhardina respectively) (Fig. 3b; Table S2) have greater PTS indices than those observed in extant taxa. Te best supported model for Bayesian ancestral state reconstruction (Fig. 4, Table S13) utilizes a delta parameter <1 (mean δ = 0.544) and estimates that the ancestral crown primate possessed a well-developed PTS (1.19), in stark contrast to all other euarchontan groups, including plesiadapiforms (0.68). Evolutionary models generated with stepwise-ftting of Ornstein-Uhlenbeck adaptive regimes accord well with the evolutionary pattern implied by ancestral state reconstruction. For extant taxa (Fig. 3a; Table S21), the base of the euarchontan tree is characterized by a low adaptive optimum for the PTS index (0.74) which is SCIENTIFIC REPORTS | (2019) 9:12341 | https://doi.org/10.1038/s41598-019-48651-x 2 www.nature.com/scientificreports/ www.nature.com/scientificreports a c Leg PTS Talus Tarsus and metatarsus Phalanges b Leg d Tarsus and Phalanges
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