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The Mechanical Origins of Arm-Swinging

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The Mechanical Origins of Arm-Swinging Journal of Human Evolution 130 (2019) 61e71 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol The mechanical origins of arm-swinging * Michael C. Granatosky a, , Daniel Schmitt b a Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA b Department of Evolutionary Anthropology, Duke University, Durham, NC, USA article info abstract Article history: Arm-swinging is a locomotor mode observed only in primates, in which the hindlimbs no longer have a Received 9 July 2018 weight bearing function and the forelimbs must propel the body forward and support the entirety of the Accepted 2 February 2019 animal's mass. It has been suggested that the evolution of arm-swinging was preceded by a shift to inverted quadrupedal walking for purposes of feeding and balance, yet little is known about the me- chanics of limb use during inverted quadrupedal walking. In this study, we test whether the mechanics of Keywords: inverted quadrupedal walking make sense as precursors to arm-swinging and whether there are Arboreal locomotion fundamental differences in inverted quadrupedal walking in primates compared to non-primate mam- Brachiation Primates mals that would explain the evolution of arm-swinging in primates only. Based on kinetic limb-loading Sloths data collected during inverted quadrupedal walking in primates (seven species) and non-primate Bats mammals (three species), we observe that in primates the forelimb serves as the primary propulsive Suspensory locomotion and weight bearing limb. Additionally, heavier individuals tend to support a greater distribution of body weight on their forelimbs than lighter ones. These kinetic patterns are not observed in non-primate mammals. Based on these findings, we propose that the ability to adopt arm-swinging is fairly simple for relatively large-bodied primates and merely requires the animal to release its grasping foot from the substrate. This study fills an important gap concerning the origins of arm-swinging and illuminates previously unknown patterns of primate locomotor evolution. © 2019 Elsevier Ltd. All rights reserved. 1. Introduction (Hunt et al., 1996; Usherwood et al., 2003). Despite the funda- mental importance of arm-swinging to the evolutionary history of Arm-swinging is a form of suspensory locomotion unique to primates, its origins remain unknown. While the adaptive advan- primates among mammals in which only the forelimbs are used for tages of suspensory locomotion have been discussed in great detail weight-support and forward propulsion. This dynamic and me- (see Grand, 1972; Cartmill and Milton, 1977; Cartmill, 1985; chanically challenging form of locomotion has evolved multiple Granatosky, 2016), no hypothesis has yet to be proposed for why times within primates: at least once in atelines (Jones, 2008; primates utilize arm-swinging while all other mammals are Rosenberger et al., 2008), once in Pygathrix (Byron and Covert, restricted to inverted quadrupedal walking. 2004; Granatosky, 2015; Byron et al., 2017), and once, if not more From a paleontological perspective, investigating the origins of times, in hominoids (Avis, 1962; Lewis, 1971; Tuttle, 1975; Larson, arm-swinging is difficult. Much of these challenges arise from the 1998). Furthermore, even anatomically non-specialized primates fact that, although there are many anatomical modifications pre- have been observed occasionally arm-swinging (Supplementary sent within the postcranial skeleton of specialized arm-swinging Online Material [SOM] Table S1). It should be noted that, primates (e.g., Johnson and Shapiro, 1998; Larson, 1998; Rein although arm-swinging is often used synonymously with brachia- et al., 2015; see list below), these features are not required to tion (e.g., Avis, 1962; Tuttle, 1975; Byron and Covert, 2004; Jones, adopt arm-swinging behavior. It is easy to recognize habitual arm- 2008), in this manuscript we reserve the term brachiation to swingers among extant and extinct taxa with their long forelimbs describe the ricochetal suspensory movements of extant gibbons and long manual digits. But the earliest instances of arm-swinging as a critical adaptive behavior may have involved a functional transition in the role of the forelimb without major anatomical change. The number of anatomically non-specialized primates * Corresponding author. observed occasionally arm-swinging (SOM Table S1) supports the E-mail address: [email protected] (M.C. Granatosky). https://doi.org/10.1016/j.jhevol.2019.02.001 0047-2484/© 2019 Elsevier Ltd. All rights reserved. 62 M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e71 notion that the ability to adopt arm-swinging locomotion does not craniocaudally elongated and dorsoventrally short spinous pro- require any particular anatomical necessity beyond a mobile cesses, dorsally oriented transverse processes, and dorsoventrally shoulder joint and the ability to flex the digits of the hand into a and mediolaterally elongated vertebral bodies (Johnson and functional hook (Granatosky, 2016). Such features are considered Shapiro, 1998; Granatosky et al., 2014). Such profound anatomical synapomorphic for primates (Larson, 1998; Bloch and Boyer, 2002; similarities have led to the as yet untested proposition that the Schmitt and Lemelin, 2002; Boyer et al., 2013); thus, all primates evolution of arm-swinging could be associated with an increase in have the potential to move by arm-swinging. Additionally, Byron body size in arboreal primates that commonly adopt inverted et al. (2017) demonstrated that there are limited mechanical solu- quadrupedal walking (Grand, 1972; Cartmill and Milton, 1977; tions to arm-swinging, and as such anatomical convergence and Cartmill, 1985). parallelism are to be expected, an idea that reflects arguments In support of this notion, it is worth noting that the relative made by Larson (1998). Such evolutionary processes make accurate importance of suspensory locomotion and posture in arboreal reconstructions of phylogenetic relatedness and trait evolution mammals' behavioral repertoires varies as a function of its body tenuous. It should also be noted that many derived postcranial weight; for larger animals it is mechanically easier to hang below a features of extant hominoids are suitable for both suspensory be- relatively small branch rather than balancing atop it (Grand, 1972; haviors and vertical climbing, so it is uncertain whether they Cartmill, 1985). In this light, it is possible to hypothesize that the evolved first as an adaptation of one of these behaviors and were evolution of arm-swinging in primates proceeds from arboreal subsequently co-opted for the other, or whether the two special- quadrupedal walking to inverted quadrupedal walking and then to ized behaviors evolved simultaneously (for a relevant example, see arm-swinging, with changes in hindlimb and forelimb function at Moya-Sol a et al., 2004; Alba et al., 2010; Alba, 2012). Taken each stage. That explanation, which is intuitively appealing, re- together, a purely paleontological approach to investigating the mains untested and is not a sufficient explanation in light of origins of arm-swinging is problematic because without clear available data. Other mammals use inverted quadrupedal walking diagnostic anatomical features linked with specific behaviors, it is in their normal locomotor repertoire (Fujiwara et al., 2011; impossible to accurately reconstruct the locomotor repertoire of Granatosky, 2016), but arm-swinging has only evolved in pri- the earliest supposed arm-swinging primates. mates. Moreover, the fact that multiple lineages of primates As complement to paleontological analysis, an experimental evolved arm-swinging independently suggests the presence of approach using extant animals has proven greatly informative in some shared mechanical precursor to arm-swinging present in all reconstructing patterns in locomotor evolution across tetrapods primate lineages and not observed in other mammals (Byron et al., (Schmitt and Lemelin, 2002; Reilly et al., 2006; Grossi et al., 2014; 2017). The questions that arise then are: do the mechanics of Nyakatura et al., 2014; Karantanis et al., 2015). Mechanically, the inverted quadrupedal walking make sense as precursors to arm- evolution of arm-swinging must have required a functional reor- swinging and are there fundamental differences in inverted ganization of the forelimb to become the primary propulsive and quadrupedal walking in primates compared to non-primate load-bearing limb (Fleagle et al., 1981; Granatosky, 2016; Byron mammals that would explain the evolution of arm-swinging in et al., 2017). This arrangement presents an especially difficult primates only? biomechanical challenge for primates, which predominantly rely Data on limb-loading patterns of primates during inverted on the hindlimb for both weight support and propulsion during quadrupedal walking are currently limited to three closely-related arboreal quadrupedal walking, climbing, and leaping (Kimura et al., strepsirrhine species. During inverted quadrupedal walking for 1979; Reynolds, 1985; Hirasaki et al.,1993; Hanna et al., 2017). Thus, these species, the forelimbs carry more body weight than the the origin of arm-swinging in primates, and not other animals, is hindlimbs and serve as the primary propulsive limb, while the simultaneously central to understanding the evolution of our order hindlimbs serve primarily braking functions (Ishida et al., 1990;
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