Chimpanzee super strength and human skeletal muscle evolution
Edited by Jill M. Slade, Michigan State University, East Lansing, MI, and accepted by Editorial Board Member C. O. Lovejoy March 31, 2017 (received for review November 29, 2016)
Significance
Chimpanzee “super strength” has been widely reported since the 1920s although a critical review of the available data suggests that the chimpanzee–human muscular performance differential is only ∼1.5 times. Some hypothesize that this differential reflects underlying differences in muscle mechanics. Here, we present direct measurements of chimpanzee skeletal muscle properties in comparison with those of humans and other terrestrial mammals. Our results show that chimpanzee muscle exceeds human muscle in maximum dynamic force and power output by ∼1.35 times. This is primarily due to the chimpanzee’s higher fast-twitch fiber content, rather than exceptional maximum isometric force or maximum shortening velocities. We suggest that muscular performance capabilities declined during hominin evolution in response to selection for repetitive, low-cost contractile behavior.
Abstract
Since at least the 1920s, it has been reported that common chimpanzees (Pan troglodytes) differ from humans in being capable of exceptional feats of “super strength,” both in the wild and in captive environments. A mix of anecdotal and more controlled studies provides some support for this view; however, a critical review of available data suggests that chimpanzee mass-specific muscular performance is a more modest 1.5 times greater than humans on average. Hypotheses for the muscular basis of this performance differential have included greater isometric force-generating capabilities, faster maximum shortening velocities, and/or a difference in myosin heavy chain (MHC) isoform content in chimpanzee relative to human skeletal muscle. Here, we show that chimpanzee muscle is similar to human muscle in its single-fiber contractile properties, but exhibits a much higher fraction of MHC II isoforms. Unlike humans, chimpanzee muscle is composed of ∼67% fast-twitch fibers (MHC IIa+IId). Computer simulations of species-specific whole-muscle models indicate that maximum dynamic force and power output is 1.35 times higher in a chimpanzee muscle than a human muscle of similar size. Thus, the superior mass-specific muscular performance of chimpanzees does not stem from differences in isometric force-generating capabilities or maximum shortening velocities—as has long been suggested—but rather is due in part to differences in MHC isoform content and fiber length. We propose that the hominin lineage experienced a decline in maximum dynamic force and power output during the past 7–8 million years in response to selection for repetitive, low-cost contractile behavior.
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Modern humans—with some exceptions—are often characterized as a weak and unathletic species compared with our closest living relatives, the chimpanzees. Whereas chimpanzees are proficient tree climbers and arborealists (1), our hominin ancestors gave up a reliance on the forest canopy after the emergence of the genus Homo (2). Subsequent evolution in brain size (3) and cognition as well as advancements in tools and other material culture (4, 5) have reduced our strict dependence on muscular strength for survival and fitness.
Since at least the 1920s, both anecdotal reports and more controlled experiments have indicated that the strength of a chimpanzee can exceed that of a human (6–12). This has led to the now long-standing proposal that chimpanzees are “super strong” compared with humans. A critical review of experiments (i.e., pulling and jumping tasks) carried out between 1923 and 2014 suggests that chimpanzee mass-specific muscular performance consistently exceeds that of humans, with a differential of about 1.5 times, on average (SI Appendix, SI Discussion). Hypotheses for the muscular basis of the chimpanzee–human performance differential have included higher isometric force-producing capabilities (6–8, 11), faster maximum shortening velocities (7, 11), and/or a different distribution of myosin heavy chain (MHC) isoforms than human skeletal muscle (10, 11). However, to date there have been no direct measurements of these parameters in the skeletal muscle of chimpanzees. Yet, if one or more of these hypotheses are correct, it would indicate a significant (and previously unappreciated) evolutionary shift in the force and/or power-producing capabilities of skeletal muscle in either Pan or Homo since these two lineages diverged about 7–8 million years ago (Mya) (13).
In this study, we present direct measurements of single-fiber contractile properties and MHC isoform distributions of chimpanzee skeletal muscle to test these hypotheses. We compare our chimpanzee data to similar data from humans and a wide range of other terrestrial mammals. The single-fiber and MHC datasets are then used to parameterize chimpanzee and human muscle models. Computer simulation of these models under matched contractile conditions permit a controlled comparison of chimpanzee and human muscular performance capabilities. Based on our results, we suggest that the maximum dynamic force and power-producing capabilities of skeletal muscle has declined during the past 7–8 million years of hominin evolution, likely due to selection for repetitive, low-cost contractile behavior.
Results
Using an isolated muscle fiber preparation, we directly measured the maximum isometric force and maximum shortening velocity of the skeletal muscle of the common chimpanzee (Pan troglodytes). Data were collected at 15 °C from fibers containing pure MHC I, IIa, and IId isoforms. The maximum isometric force (Po) of chimpanzee skeletal muscle ranged from 96 kN⋅m−2 to 150 kN⋅m−2, and the maximum shortening velocity (Vo) ranged from 0.64 to 4.96 L⋅s−1, depending on MHC type (Fig. 1 and SI Appendix, SI Methods and Tables S1 and S2). These results, which are taken to be representative of limb and trunk skeletal muscle in general, indicate that chimpanzee muscle is similar to humans and other terrestrial mammals in its single-fiber contractile properties (Fig. 1 D and E). Indeed, the Po and Vo of chimpanzee muscle are not significantly different from humans (P > 0.05, one sample t test) and are generally consistent with expectations based on body size scaling (Fig. 1 F and G). Given these cellular-level results, humans and chimpanzees can be expected to exhibit commonalities in the molecular properties that affect single-fiber performance, such as actin–myosin kinetics.
Fig. 1.
We measured the distribution of MHC isoforms within 35 pelvis and hind-limb muscles of chimpanzees and found a balanced distribution of MHC I, IIa, and IId on average (Fig. 2 and SI Appendix, Table S3). This is in marked contrast to humans, who exhibit a significant bias toward MHC I fibers in these same muscles and throughout the limbs and trunk overall (14, 15). Although the genetic basis of skeletal muscle MHC isoform specification is an active area of research (e.g., ref. 16), the magnitude of the chimpanzee–human contrast in MHC I fibers appears to exceed the more modest shifts that may be induced through intense athletic training (∼10–15%) (17, 18). Furthermore, characterization of fiber-type distributions in the muscles of lemurs, galagos, and macaques suggests that a predominance of MHC II (IIa + IId) isoforms (i.e., fast fibers) is common among primates, as well as other terrestrial mammals (SI Appendix, SI Methods and Table S5). Indeed, the slow loris (Nycticebus coucang) is the only other mammal measured to date with a predominance of slow fibers across its skeletal muscles. Thus, we suggest that the high percentage of MHC I fibers in human skeletal muscle is a derived trait within the hominin lineage, rather than a characteristic of African apes or other nonhuman primates in general.
Fig. 2.
A salient architectural difference between chimpanzee and human skeletal muscle is that chimpanzees have longer muscle fibers (both in absolute and relative length) (19). Longer muscle fibers have a broader force–length relation that may enhance the dynamic force, work, and power capabilities of a muscle–tendon unit (20). Therefore, to estimate the net interacting effects of Po, Vo, MHC distribution, and muscle fiber length on maximum dynamic muscle force and power output in vivo, we designed Hill-type “chimpanzee muscle” and “human muscle” models that reflected the parameter differences measured herein and elsewhere (14, 15, 19). Using computer simulations, we determined the maximum dynamic force and power-producing capabilities of these models at the whole-muscle level.
Simulation of a single-burst maximal contraction against a heavy, inertial load predicted that chimpanzee muscle would have a 1.35 times higher maximum dynamic force [chimpanzee (C): 125.6 kN⋅m−2; human (H): 93.0 kN⋅m−2] and power (C: 220.7 W⋅kg−1; H: 163.8 W⋅kg−1) output than human muscle (Fig. 3). Similarly, simulation of a series of cyclical contractions predicted a 1.34 times higher maximum power output from chimpanzee muscle when the control variables governing muscle excitation and contractile frequency were optimized (C: 172.9 W⋅kg−1; H: 129.2 W⋅kg−1). These results suggest that the larger fraction of MHC II fibers and the longer muscle fiber lengths characteristic of chimpanzee skeletal muscle will increase their dynamic force and power-producing capabilities overall. If a chimpanzee-like or macaque-like phenotype characterized the skeletal muscles of the last common ancestor of chimpanzees and humans, then the maximum dynamic force and power-producing capabilities of hominin skeletal muscles have declined over the past 7–8 million years (13).
Fig. 3.
Discussion
The 1.35 times differential predicted here seems modest compared with popular accounts of “super strength” in chimpanzees. However, a critical review of the controlled dynamic force- and power-limiting experiments (6–11) that have attempted to quantify this performance differential indicates that, on a mass-specific basis, chimpanzees outperform humans in pulling and jumping tasks by about 1.5 times on average (SI Appendix, SI Discussion). Although our simulations do not reproduce the earlier experimental designs in detail, the close approximation of our results to the 1.5 times average suggests that muscle mechanics—MHC isoform content, in particular—accounts for much, but not necessarily all, of the measured chimpanzee–human performance differential. Muscle “static strength,” defined as maximum isometric force-producing capabilities (Po), is not significantly different between these two species and therefore does not contribute to their performance differential (6–8, 10). Of course, linking muscle mechanics to whole-body performance tasks is difficult due to the complexities that arise from the many muscle–tendon units with differing excitations acting across joints with variable leverages. For example, in maximal pulling, chimpanzee performance may benefit from the larger moment arms of some of their fore (upper) limb musculature (19). More detailed musculoskeletal modeling and integrated experimental-simulation work would be required to determine the contributions of these and other possible factors to the remaining 1.15 differential on average. This would also permit a more precise assessment of the contribution of muscle mechanics to the task-specific details that underlie the full range of measured chimpanzee–human performance differentials (i.e., 1.20–2.05 times across studies, SI Appendix, SI Discussion).
It has also been hypothesized that humans have greater cortical and/or spinal inhibition of maximal muscle recruitment than chimpanzees, thereby limiting their muscular performance capabilities in comparison (12). If true, this would further increase the chimpanzee–human differential; however, we are unaware of any data that directly support this “inhibition hypothesis.” Instead, experimental studies indicate that humans are capable of complete (or near complete) voluntary activation of their musculature when assigned a maximal performance task (e.g., ref. 21). Thus, the expectation that both species are capable of optimizing their neuromuscular control strategies in response to the mechanical demands of a given task appears to be more consistent with available data.
Our integrated experiment-simulation results indicate that the skeletal muscle of chimpanzees is better suited for maximum dynamic force and power output than that of humans, perhaps reflecting the chimpanzee’s greater reliance on tree climbing and suspension for survival and fitness. Furthermore, we propose that the higher fraction of MHC I fibers and shorter muscle fiber lengths in human skeletal muscle are adaptive for repetitive, low-cost contractile behavior. MHC I fibers have high mitochondrial volume densities and capillary-fiber contact length (17), which facilitate O2 diffusion; short fibers can reduce the cost of isometric force output due to a reduction in the muscle volume to cross-sectional area ratio (22). A high fraction of MHC I fibers can also reduce fatigue by limiting the muscle’s reliance on glycogen and other intracellular substrates during contractions (17), which permits more frequent muscle activations per day in the aerobic range. Indeed, the large muscle masses (both in absolute and relative terms) in human hind (lower) limbs (19, 23, 24) further enhance our aerobic range during bipedalism (25). Taken together, our results provide an explanation of how chimpanzees can outperform humans in some muscle-driven tasks (e.g., maximal pulling and jumping) (6–11), but not in others (e.g., metabolic cost of walking) (22). Our results may also account for the exceptionally high metabolite concentrations found in human muscle compared with chimpanzee muscle (11).
These data suggest that, although intrinsic muscle contractile properties appear to be conserved, the hominin lineage was characterized by an increase in MHC I isoform content and a decrease in muscle fiber length (19), both of which can impact a range of muscle-driven tasks. The timing of shifts in MHC content and fiber length within the hominin lineage is difficult to establish; however, we anticipate these shifts to have been concurrent with major transitions in locomotor behavior, increases in daily travel distances, increases in home range size, or some combination thereof. The early hominin Ardipithecus ramidus is likely similar to chimpanzees and other African apes in its body mass to hind-limb length (26), suggesting that this species still allocated a smaller fraction of its total muscle mass to its hind limbs than humans. The earliest australopithecines (i.e., Australopithecus anamensis and Australopithecus afarensis) exhibit changes in the pelvis and hind-limb skeleton from Ar. ramidus (27, 28), suggesting an adaptive shift toward greater overground locomotion about 4 Mya. However, the proximate ecological trigger for this transition remains elusive (29). By about 1.8 Mya, Homo erectus had likely reduced tree climbing to contemporary hunter-gatherer levels while increasing daily travel distances and home range size, perhaps aimed at enhancing diet quality through the inclusion of meat or other low-abundance foods (26, 30, 31).
Contrary to some long-standing hypotheses (6–11), evolution has not altered the basic force, velocity, or power-producing capabilities of skeletal muscle cells to induce the marked differences between chimpanzees and humans in walking, running, climbing, and throwing capabilities (22, 30, 31). This is a significant, but previously untested assumption. Instead, natural selection appears to have altered more global characteristics of muscle tissue, such as MHC distributions and muscle fiber lengths. Our integrated experiment-simulation results indicate that these changes have led to a general reduction in maximum dynamic force and power-producing capabilities; however, they have enhanced metabolic characteristics and endurance capacities of human muscle. Today, intensive athletic training can mitigate some of our inherent limitations in maximal muscle performance, but primarily through force enhancement via skeletal muscle hypertrophy (e.g., ref. 32). More generally, although higher levels of anatomical organization, such as the size and shape of muscle, tendon, and bone have been the main targets of evolutionary processes, hominin muscle dynamic force and power-producing capabilities have also been altered since the Pan and Homo lineages diverged 7–8 million years ago.
Materials and Methods
Animals.
Muscle fibers were sampled from three young male common (P. troglodytes) chimpanzees (age: 5.5 ± 0.2 y; mass: 26.5 ± 6.7 kg). All animals were housed in an American Association of Animal Laboratory Care International accredited space with facilities that allowed them to engage in normal social and locomotor behaviors. They had a dedicated animal handler and a staff of technicians who played and interacted with them daily. All of our procedures followed the guidelines of the Stony Brook University Institutional Animal Care and Use Committee.
Muscle Fiber Preparation.
Small samples of skeletal muscle (about 1 cm × 0.5 cm × 0.5 cm) were removed from the musculus (m.) vastus lateralis and m. gastrocnemius lateralis of the right hind limb of each animal while under general anesthesia. The samples were immediately immersed in cold relaxing solution with 50% (vol/vol) glycerol for overnight transport to The Ohio State University. All of the solutions used for the storage of bundles and measurements of single-fiber contractile properties followed previous experiments (33). Upon arrival, muscle bundles were dissected in a dish containing cold relaxing solution and were stored in fresh relaxing solution with 50% glycerol at −20 °C. Single fibers were subsequently isolated by dissection from the bundles for force and velocity measurements. Single, isolated fibers were mounted in a temperature-controlled experimental chamber, maintained at 15 °C. The fiber was connected at one end to a servo-controlled torque motor (model 322C, Aurora Scientific) and, at the other end, to an isometric force transducer (model 403, Aurora Scientific). The motor and transducer were attached to three-way positioners. The length of the mounted fiber was adjusted by moving the motor or transducer to set the resting striation spacing (i.e., sarcomere length). Striation spacing was determined using a microscope digital camera and image analysis software. Fiber width and depth were measured and fiber cross-sectional area (CSA) was calculated, assuming an ellipsoidal cross-section.
Recording Force and Velocity.
The fiber was activated by transferring it to a well in the experimental chamber containing a calcium ion (Ca)-activating solution. The force/pCa (−log[Ca]) relationship was determined in an initial set of fibers to determine the maximally activating solution for subsequent force and velocity measurements. The sarcomere length for these measurements was set to 2.40–2.50 μm. The force/pCa relationship indicated that pCa 4.0 was maximally activating. The active force generated in pCa 4.0 solution was normalized by fiber CSA to calculate the Po. The Vo was measured using the “slack test” (34). Each fiber was activated during a series of exposures to a pCa 4.0 solution. A known amount of slack was rapidly (within ∼2 ms) introduced into the fiber during each exposure by movement of the motor arm after steady isometric force was attained and the time required to take up the slack was measured from the force record (35). Each fiber was immediately stored at −40 °C until analysis of MHC isoform composition to determine the fiber type.
MHC Isoforms.
The MHC isoform(s) expressed in each fiber was identified using SDS/PAGE. The composition, preparation, staining, and densitometric scanning of the gels were identical to those described previously (36). The amount of each MHC isoform in fibers that expressed more than one isoform was calculated as a percentage of the total amount of MHC. The three MHC isoforms that were detected on protein gels were identified by mass spectrometry. MHC gel bands were excised from a Coomassie Blue-stained gel and submitted to the Campus Chemical Instrument Center at The Ohio State University to obtain identification by liquid chromatography–tandem mass spectrometry. The slowest migrating band was identified as fast-type MHC-IId, with a MOWSE score of 27,153, based on 741 peptide matches. The band with intermediate electrophoretic mobility was identified as fast-type MHC-IIa, with a MOWSE score of 23,010, based on 732 peptide matches. The fastest migrating band was identified as slow-type MHC-I, with a MOWSE score of 23,070, based on 694 peptide matches.
The MHC distribution was further determined in samples (10–20 mg) of 35 pelvis and hind-limb muscles from three common chimpanzee specimens not involved in the muscle contractile property measurements. Before each chimpanzee’s death (of natural causes), it had been living at a zoo or research institution. The cadaveric remains of each chimpanzee were kept fresh frozen at −20 °C after death until dissection. For each chimpanzee pelvis and/or hind limb, the skin and fascia were removed; individual muscles were identified and dissected free from their attachments. Following the work of others (14), a 2-cm × 0.5-cm × 0.5-cm sample was then taken from each muscle and used to determine MHC isoform composition in the same manner as for the single fibers (SI Appendix, Table S3).
Muscle Modeling.
Hill-type muscle models were used to investigate the combined effects of Po, Vo, MHC isoform distributions, and fiber length on maximum dynamic force and power output at the whole-muscle level. The chimpanzee and human models each included species-specific force–velocity, force–length, and activation–deactivation relations, scaled from the generic Thelen2003Muscle (37) model implemented in the OpenSim musculoskeletal modeling environment (38). Po and Vmax parameters were assigned the measured Po and Vo values scaled to normal operating temperature (∼35 °C) (SI Appendix, SI Methods and Table S4). The curvature of the force–velocity relationship (Arel) and activation–deactivation time constants (τact, τdeact) were calculated based on the average fraction of MHC II (fast-twitch) fibers determined for each species (C: 67%, H: 40%) (39). The distribution of fast-twitch fibers in humans represents an average of recent MHC measurements (i.e., MHC IIa+IIx) (14) and older immunohistochemistry measurements [i.e., fast oxidative glycolytic (FOG) + fast glycolytic (FG)] (15). To isolate the effects of muscle on performance, the simulations were conducted using rigid tendons with fiber pennation angles set to 0°. This ensured that the fiber strain matched the muscle–tendon unit strain in the simulations.
A salient architectural difference between chimpanzee and human skeletal muscle is that chimpanzees possess longer muscle fibers on average (19). Chimpanzee (23) and human (24) musculoskeletal models were used to calculate the average relative fiber length [i.e., Lo/(Lo + Ls)] for each species and determine the magnitude of the interspecific difference. The two musculoskeletal models include all of the same muscles, except that the human model lacks an m. obturator externus and an m. gluteus maximus superficialis, which is distinct from the m. gluteus maximus in all humans (23). Based on the pelvis and hind-limb muscle–tendon units in the two musculoskeletal models, relative muscle fiber length was 0.59 ± 0.21 in chimpanzees and 0.44 ± 0.25 in humans. This indicates that chimpanzee muscle fibers constitute an ∼15% longer fraction of muscle–tendon unit length on average. We incorporated this difference into our chimpanzee model by increasing relative fiber length from an initial value of 0.43 to a value of 0.58 (SI Appendix, Table S4).
Muscle Model Simulations.
The performance of each muscle model was simulated under two conditions. For the first condition, the muscle was mounted between a fixed clamp and a mobile, 500-kg inertial load on a frictionless surface (Fig. 3). The inertial load had one degree of freedom, which allowed the muscle to shorten from its optimal length (Lo) thereby accelerating the mass from rest. This simple design approximates the dynamics of a single-burst muscle-powered acceleration, as in a maximal pulling or jumping task. For each muscle model and simulation, the muscle was maximally excited and the dynamic simulation was run for 0.4 ms. The duration of the simulation was sufficient to elicit the maximum dynamic force and power output of each muscle model.
For the second condition, an experimental ergometer was modeled as a muscle mounted between a fixed clamp and mobile clamp on a frictionless surface (Fig. 3). The mobile clamp had one degree of freedom that could be slid to shorten or lengthen the muscle from its Lo. This design was intended to mimic the in vitro preparation used for determining the maximum power-producing capabilities of muscle in cyclical contractions (40). For each muscle model, the mobile clamp was prescribed a sinusoidal motion that shortened and lengthened the muscle by 0.2 Lo, centered on Lo, over three full cycles. This strain amplitude is similar to direct in vivo measurements of muscle fiber strain during a range of high-power output activities (e.g., refs. 41–43). We used a simulated annealing algorithm (44) to optimize a set of control variables that maximized the average net power of the last full strain cycle. Specifically, the control variables included the muscle excitation on (ton) and off (toff) times, as well as the muscle strain cycle frequency (f).
For each muscle model, the optimization problem was configured and solved using the OpenSim-MATLAB application programming interface (38). Maximum force and power outputs were expressed in kN⋅m−2 and W⋅kg−1, respectively. The muscle area (m2) and mass (kg) divisors were computed using the new chimpanzee Po values scaled to normal operating temperature and then weighted by MHC isoform distribution for each species (C: 262 kN⋅m−2; H: 248 kN⋅m−2) (SI Appendix, SI Methods and Table S4). In all simulations, maximum muscle force was fixed at 2255.4 N, which approximates a human m. vastus lateralis (24).
Statistics.
Measurements of the single-muscle-fiber contractile properties (i.e., Po, Vo) of chimpanzees were evaluated for the effect of MHC isoform composition using an analysis of variance (ANOVA) with pairwise comparisons between MHC isoforms. The chimpanzee single-muscle-fiber properties were then compared with similar data for humans and other mammals culled from published studies of single muscle fibers at 15 °C. The human dataset includes a range of populations and ages (SI Appendix, Table S1), with human subject data from our laboratory falling well within this range (SI Appendix, SI Methods and Fig. S2); the mammalian dataset ranges in size from mice (0.025 kg) to rhinos (2,500 kg) (SI Appendix, Table S2). One-sample t tests were used to compare the chimpanzee Po and Vo means to the human mean values from the literature. The scaling relationships of log10 Po and Vo with log10 body mass were evaluated using phylogenetic generalized least squares (pGLS). The phylogenetic structure of the analyzed species was taken from published mammalian trees (45–47). The pGLS parameters were estimated using the Comparative Analyses of Phylogenetics and Evolution in R package (48) with the parameter lambda (λ) fixed at 0 (star phylogeny) and 1 (Brownian motion) and empirically estimated using a maximum-likelihood (ML) approach. The three different model fits (i.e., λ = 0, 1, ML) were compared using a likelihood-ratio test. In all cases, the log-likelihood ratio test indicated that λ = 0 (star phylogeny) provided a statistically equivalent fit to the other two models and therefore was our preferred model for size scaling of all mammalian single-muscle-fiber contractile properties.
The distribution of MHC isoforms within 35 pelvis and hind-limb muscles of chimpanzees (SI Appendix, Table S3) was compared using an ANOVA. Independent sample t tests were used to conduct pairwise comparisons between the average fraction of MHC I or slow-twitch fibers in chimpanzees and humans, as well as between the relative muscle fiber length in chimpanzees and humans. For the MHC I content and relative fiber-length comparisons, the same 35 muscles were compiled for the chimpanzee and human samples, with the exceptions that m. gluteus minimus MHC content was not reported in Tirrell et al. (14) and m. obturator externus fiber length was not included in Arnold et al. (24). Exclusion of these muscles from the chimpanzee samples did not alter the statistical significance of the t-test results.
Acknowledgments
We thank Dr. T. Zimmerman, J. Rooney, K. Lasek, E. Moyer, and L. Yohe for assistance with data collection; B. Demes and D. Schmitt for providing chimpanzee cadaveric material; C. Rose for muscle model illustrations; S. Zack for helpful input on mammalian phylogenetics; and M. Miller and J. Stern for comments on earlier versions of the manuscript. Funding was provided by the National Science Foundation (BCS-0935321 to M.C.O. and S.G.L. and BCS-0935327 to B.R.U.).
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Published online: June 26, 2017
Published in issue: July 11, 2017
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Acknowledgments
We thank Dr. T. Zimmerman, J. Rooney, K. Lasek, E. Moyer, and L. Yohe for assistance with data collection; B. Demes and D. Schmitt for providing chimpanzee cadaveric material; C. Rose for muscle model illustrations; S. Zack for helpful input on mammalian phylogenetics; and M. Miller and J. Stern for comments on earlier versions of the manuscript. Funding was provided by the National Science Foundation (BCS-0935321 to M.C.O. and S.G.L. and BCS-0935327 to B.R.U.).
Notes
This article is a PNAS Direct Submission. J.M.S. is a guest editor invited by the Editorial Board.
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The authors declare no conflict of interest.
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