Trabecular bone variation in the gorilla calcaneus.

ankle arboreality foot terrestriality

Journal

American journal of biological anthropology
ISSN: 2692-7691
Titre abrégé: Am J Biol Anthropol
Pays: United States
ID NLM: 101770171

Informations de publication

Date de publication:
17 Apr 2024
Historique:
revised: 15 02 2024
received: 24 08 2023
accepted: 02 04 2024
medline: 18 4 2024
pubmed: 18 4 2024
entrez: 17 4 2024
Statut: aheadofprint

Résumé

Calcaneal external shape differs among nonhuman primates relative to locomotion. Such relationships between whole-bone calcaneal trabecular structure and locomotion, however, have yet to be studied. Here we analyze calcaneal trabecular architecture in Gorilla gorilla gorilla, Gorilla beringei beringei, and G. b. graueri to investigate general trends and fine-grained differences among gorilla taxa relative to locomotion. Calcanei were micro-CT scanned. A three-dimensional geometric morphometric sliding semilandmark analysis was carried out and the final landmark configurations used to position 156 volumes of interest. Trabecular thickness (Tb.Th), trabecular spacing (Tb.Sp), and bone volume fraction (BV/TV) were calculated using the BoneJ plugin for ImageJ and MATLAB. Non-parametric MANOVAs were run to test for significant differences among taxa in parameter raw values and z-scores. Parameter distributions were visualized using color maps and summarized using principal components analysis. There are no significant differences in raw BV/TV or Tb.Th among gorillas, however G. b. beringei significantly differs in z-scores for both parameters (p = <0.0271). All three taxa exhibit relatively lower BV/TV and Tb.Th in the posterior half of the calcaneus. This gradation is exacerbated in G. b. beringei. G. b. graueri significantly differs from other taxa in Tb.Sp z-scores (p < 0.001) indicating a different spacing distribution. Relatively higher Tb.Th and BV/TV in the anterior calcaneus among gorillas likely reflects higher forces associated with body mass (transmitted through the subtalar joint) relative to forces transferred through the posterior calcaneus. The different Tb.Sp pattern in G. b. graueri may reflect proposed differences in foot positioning during locomotion.

Identifiants

pubmed: 38631677
doi: 10.1002/ajpa.24939
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e24939

Subventions

Organisme : Division of Behavioral and Cognitive Sciences
ID : BCS-1317047
Organisme : Division of Behavioral and Cognitive Sciences
ID : BCS-1824630

Informations de copyright

© 2024 The Authors. American Journal of Biological Anthropology published by Wiley Periodicals LLC.

Références

Adams, D. C., & Otárola‐Castillo, E. (2013). Geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399.
Addison, B. J., & Lieberman, D. E. (2020). Assessing patterns of variation in BV/TV in the calcaneus and C2 vertebra of Gorilla gorilla, pan troglodytes, and populations of Homo sapiens from the Pleistocene and Holocene that differ in physical activity levels. American Journal of Physical Anthropology, 173, 337–349.
Athavale, S. A., Joshi, S. D., & Joshi, S. S. (2010). Internal architecture of calcaneus: Correlations with mechanics and pathoanatomy of calcaneal fractures. Surgical and Radiologic Anatomy, 32, 115–122.
Bajraliu, M., Walley, K. C., & Kwon, J. Y. (2016). Rationale for the hypodense calcaneal region of Ward's neutral triangle. The Orthopaedic Journal at Harvard Medical School, 17, 63–67.
Barak, M. M., Lieberman, D. E., & Hublin, J.‐J. (2011). A Wolff in sheep's clothing: Trabecular bone adaptation in response to changes in joint loading orientation. Bone, 49, 1141–1151.
Biewener, A. A., Fazzalari, N. L., Konieczynski, D. D., & Baudinette, R. V. (1996). Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone, 19, 1–8. https://doi.org/10.1016/8756-3282(96)00116-0
Boskey, A. L., & Imbert, L. (2017). Bone quality changes associated with aging and disease: A review. Annals of the New York Academy of Sciences, 1410, 93–106.
Boyle, E. K., McNutt, E. J., Sasaki, T., Suwa, G., Zipfel, B., & DeSilva, J. M. (2018). A quantification of calcaneal lateral plantar process position with implications for bipedal locomotion in Australopithecus. Journal of Human Evolution., 123, 24–34. https://doi.org/10.1016/j.jhevol.2018.05.008
Burgess, M. L., McFarlin, S. C., Mudakikwa, A., Cranfield, M. R., & Ruff, C. B. (2018). Body mass estimation in hominoids: Age and locomotor effects. Journal of Human Evolution, 115, 36–46.
Canington, S. L. (2018). Gorilla beringei (primates: Hominidae). Mammalian Species, 50, 119–133.
Canington, S. L., Sylvester, A. D., Burgess, M. L., Junno, J.‐A., & Ruff, C. B. (2018). Long bone diaphyseal shape follows different ontogenetic trajectories in captive and wild gorillas. American Journal of Physical Anthropology, 167, 366–376.
Carlson, K. J. (2005). Investigating the form‐function interface in African apes: Relationships between principal moments of area and positional behaviors in femoral and humeral diaphyses. American Journal of Physical Anthropology, 127, 312–334.
Casimir, M. J. (1975). Feeding ecology and nutrition of an eastern gorilla group in the Mt. Kahuzi region (République du Zaïre). Folia Primatologica, 24, 81–136.
Chirchir, H., Ruff, C. B., Junno, J.‐A., & Potts, R. (2017). Low trabecular bone density in recent sedentary modern humans. American Journal of Physical Anthropology, 162, 550–560.
Collyer, M. L., Sekora, D. J., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high‐dimensional data. Heredity, 115, 357–365.
Colombo, A., Stephens, N. B., Tsegai, Z. J., Bettuzzi, M., Morigi, M. P., Belcastro, M. G., & Hublin, J.‐J. (2019). Trabecular analysis of the distal radial metaphysis during the Acquisition of Crawling and Bipedal Walking in childhood: A preliminary study. Bulletins et Mémoires de la Société d'Anthropologie de Paris, 31(1–2), 43–51.
Currey, J. D. (2013). Bones: Structure and mechanics. Princeton University Press.
Damien, C., Felix, N., Giarrusso, A. J., Veronica, V., & Stoinski, T. S. (2014). Mountain gorilla ranging patterns: Influence of group size and group dynamics. American Journal of Primatology, 76, 730–746.
DeMars, L. J. D., Stephens, N. B., Saers, J. P. P., Gordon, A., Stock, J. T., & Ryan, T. M. (2021). Using point clouds to investigate the relationship between trabecular bone phenotype and behavior: An example utilizing the human calcaneus. American Journal of Human Biology, 33, e23468.
DeSilva, J., McNutt, E., Benoit, J., & Zipfel, B. (2019). One small step: A review of Plio‐Pleistocene hominin foot evolution. American Journal of Physical Anthropology, 168, 63–140.
Doran, D. M. (1996). Comparative positional behavior of the African apes. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great Ape Societies (pp. 213–224). Cambridge University Press.
Doran, D. M. (1997). Ontogeny of locomotion in mountain gorillas and chimpanzees. Journal of Human Evolution, 32, 323–344.
Doran, D. M., & McNeilage, A. (1998). Gorilla ecology and behavior. Evolutionary Anthropology: Issues, News, and Reviews, 6, 120–131.
Doran‐Sheehy, D. M., Greer, D., Mongo, P., & Schwindt, D. (2004). Impact of ecological and social factors on ranging in western gorillas. American Journal of Primatology, 64, 207–222.
Doube, M., Kłosowski, M. M., Arganda‐Carreras, I., Cordelières, F. P., Dougherty, R. P., Jackson, J. S., Schmid, B., Hutchinson, J. R., & Shefelbine, S. J. (2010). BoneJ: Free and extensible bone image analysis in ImageJ. Bone, 47, 1076–1079.
Doube, M., Kłosowski, M. M., Wiktorowicz‐Conroy, A. M., Hutchinson, J. R., & Shefelbine, S. J. (2011). Trabecular bone scales allometrically in mammals and birds. Proceedings of the Royal Society of London B: Biological Sciences, 278, 3067–3073. rspb20110069.
Druelle, F., Berthet, M., & Quintard, B. (2019). The body center of mass in primates: Is it more caudal than in other quadrupedal mammals? American Journal of Physical Anthropology, 169, 170–178.
Dunmore, C. J., Kivell, T. L., Bardo, A., & Skinner, M. M. (2019). Metacarpal trabecular bone varies with distinct hand‐positions used in hominid locomotion. Journal of Anatomy, 235, 45–66.
Dunn, R. H., Tocheri, M. W., Orr, C. M., & Jungers, W. L. (2014). Ecological divergence and talar morphology in gorillas. American Journal of Physical Anthropology, 153, 526–541.
Eriksen, E. F., & Glerup, H. (2000). Pathogenesis of osteoporosis. In Obrant, K. (eds.) Management of Fractures in Severely Osteoporotic Bone, pp, 13–32. Springer.
Eriksen, E. F., Mosekilde, L., & Melsen, F. (1985). Trabecular bone remodeling and bone balance in hyperthyroidism. Bone, 6, 421–428.
Fajardo, R. J., & Müller, R. (2001). Three‐dimensional analysis of nonhuman primate trabecular architecture using micro‐computed tomography. American Journal of Physical Anthropology, 115, 327–336. https://doi.org/10.1002/ajpa.1089
Fajardo, R. J., Müller, R., Ketcham, R. A., & Colbert, M. (2007). Nonhuman anthropoid primate femoral neck trabecular architecture and its relationship to locomotor mode. The Anatomical Record, 290, 422–436.
Fatica, L. M., Almécija, S., McFarlin, S. C., & Hammond, A. S. (2019). Pelvic shape variation among gorilla subspecies: Phylogenetic and ecological signals. Journal of Human Evolution, 137, 102684.
FEI Visualization Sciences Group. (2015). Avizo Lite 9.0.1. Hillsboro: FEI Company.
Figus, C., Sorrentino, R., Carlson, K. J., Colombo, A., Bortolini, E., Bernardini, F., Erjavec, I., Jajdu, T., Szeniczey, T., Mateovics‐Lászlo, Pap, I., Tuniz, C., Novak, M., Belcastro, M. G., Ryan, T. M., & Benazzi, S. (2023). Becoming adults: Exploring late ontogeny of the human talus. Frontiers in Ecology and Evolution, 11, 1205277.
Figus, C., Stephens, N. B., Sorrentino, R., Bortolini, E., Arrighi, S., Lugli, F., Marciani, G., Oxilia, G., Romandini, M., Silvestrini, S., Baruffaldi, F., Belcastro, M. G., Bernardini, F., Erjavec, I., Festa, A., Hajdu, T., Mateovics‐László, O., Novak, M., Pap, I., … Benazzi, S. (2022). Human talar ontogeny: Insights from morphological and trabecular changes during postnatal growth. American Journal of Biological Anthropology, 179(2), 211–228.
Gebo, D. L. (1992). Plantigrady and foot adaptation in African apes: Implications for hominid origins. American Journal of Physical Anthropology, 89, 29–58.
Gefen, A., & Seliktar, R. (2004). Comparison of the trabecular architecture and the isostatic stress flow in the human calcaneus. Medical Engineering & Physics, 26, 119–129.
Giddings, V. L., Beupré, G. S., Whalen, R. T., & Carter, D. R. (2000). Calcaneal loading during walking and running. Medicine & Science in Sports & Exercise, 32, 627–634.
Gierse, H. (1976). The cancellous structure in the calcaneus and its relation to mechanical stressing. Anatomy and Embryology, 150, 63–83.
Glatt, V., Canalis, E., Stadmeyer, L., & Bouxsein, M. L. (2007). Age‐related changes in trabecular architecture differ in female and male C57BL/6J mice. Journal of Bone and Mineral Research, 22, 1197–1207.
Goodall, A. G., & Groves, C. P. (1977). The conservation of eastern gorillas. In H. R. M. P. Ranier & G. H. Bourne (Eds.), Primate Conservation (pp. 599–637). Academic Press.
Gower, J. C. (1975). Generalized Procrustes analysis. Psychometrika, 40, 33–51.
Gross, T., Kivell, T. L., Skinner, M. M., Nguyen, H., & Pahr, D. H. (2014). Holistic analysis of bone. Palaeontologia Electronica, 17, 1.
Groves, C. P. (1971). Distribution and place of origin of the gorilla. Man, 6, 44–51.
Groves, C. P. (2001). Primate taxonomy. Smithsonian Institution.
Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). Springer.
Hanna, J. B., & Schmitt, D. (2011). Locomotor energetics in primates: Gait mechanics and their relationship to the energetics of vertical and horizontal locomotion. American Journal of Physical Anthropology, 145, 43–54.
Harper, C. M., Roach, C. S., Goldstein, D. M., & Sylvester, A. D. (2023). Morphological variation of the pan talus relative to that of gorilla. American Journal of Biological Anthropology, 184, 545–563.
Harper, C. M., Ruff, C. B., & Sylvester, A. D. (2021a). Calcaneal shape variation in humans, nonhuman primates, and early hominins. Journal of Human Evolution, 159, 103050.
Harper, C. M., Ruff, C. B., & Sylvester, A. D. (2021b). Gorilla calcaneal morphological variation and ecological divergence. American Journal of Physical Anthropology, 174, 49–65.
Harper, C. M., Ruff, C. B., & Sylvester, A. D. (2022). Scaling and relative size of the human, nonhuman ape, and baboon calcaneus. The Anatomical Record, 305, 100–122.
Harrigan, T. P., Jasty, M., Mann, R. W., & Harris, W. H. (1988). Limitations of the continuum assumption in cancellous bone. Journal of Biomechanics, 21, 169–275.
Hirasaki, E., Kumakura, H., & Matano, S. (1993). Kinesiological characteristics of vertical climbing in Ateles and Macaca fuscata. Folia Primatologica, 61, 148–156.
Hirasaki, E., Kumakura, H., & Matano, S. (1995). Electromyography of 15 limb muscles in Japanese macaques (Macaca fuscata) during vertical climbing. Folia Primatologica, 64, 218–224.
Hirasaki, E., Kumakura, H., & Matano, S. (2000). Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque. American Journal of Physical Anthropology, 113, 455–472.
Hirasaki, E., Matano, S., Nakano, Y., & Ishida, H. (1992). Vertical climbing in Ateles geoffroyi and Macaca fuscata and its comparative neurological background. In S. Mataon, R. D. Tuttle, H. Ishida, & M. Goodman (Eds.), Topics in primatology Vol. 3: Evolutionary biology, reproductive endocrinology, and virology (pp. 156–165). University of Tokyo Press.
Huiskes, R., Ruimerman, R., Van Lenthe, G. H., & Janssen, J. D. (2000). Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature, 405, 704–706.
Inouye, S. E. (1992). Ontogeny and allometry of African ape manual rays. Journal of Human Evolution, 23, 107–138.
Jabbour, R. S., & Pearman, T. L. (2016). Geographic variation in gorilla limb bones. Journal of Human Evolution, 95, 68–79.
Jacobs, C. R. (2000). The mechanobiology of cancellous bone structural adaptation. Journal of Rehabilitation Research & Development, 37, 209–216.
Jensen, N. C., Madsen, L. P., & Linde, F. (1991). Topographical distribution of trabecular bone strength in the human os calcanei. Journal of Biomechanics, 24, 49–55.
Jensen‐Seaman, M. I., & Kidd, K. K. (2001). Mitochondrial DNA variation and biogeography of eastern gorillas. Molecular Ecology, 10, 2241–2247.
Jungers, W. L. (1988). Relative joint size and hominoid locomotor adaptation with implications for the evolution of hominid bipedalism. Journal of Human Evolution, 17, 247–265.
Kidd, R. (1999). Evolution of the rearfoot. A model of adaptation with evidence from the fossil record. Journal of the American Podiatric Medical Association, 89, 2–17.
Kirchhoff, C., Braunstein, V., Milz, S., Sprecher, C. M., Kirchhoff, S., Graw, M., Imhoff, A. B., & Hinterwimmer, S. (2012). Age and gender as determinants of the bone quality of the greater tuberosity: A HR‐pQCT cadaver study. BMC Musculoskeletal Disorders, 13, 221.
Kivell, T. L. (2016). A review of trabecular bone functional adaptation: What have we learned from trabecular analyses in extant hominoids and what can we apply to fossils? Journal of Anatomy, 228, 569–594.
Kivell, T. L., Skinner, M. M., Lazenby, R., & Hublin, J.‐J. (2011). Methodological considerations for analyzing trabecular architecture: An example from the primate hand. Journal of Anatomy, 218, 209–225.
Knigge, R. P., Tocheri, M. W., Orr, C. M., & Mcnulty, K. P. (2015). Three‐dimensional geometric morphometric analysis of talar morphology in extant gorilla taxa from highland and lowland habitats. The Anatomical Record, 298, 277–290.
Kuo, S., Desilva, J. M., Devlin, M. J., Mcdonald, G., & Morgan, E. F. (2013). The effect of the Achilles tendon on trabecular structure in the primate calcaneus. The Anatomical Record, 296, 1509–1517.
Langergraber, K. E., Prüfer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K., Inoue, R., Inoue‐Muruyama, M., Mitani, J. C., Muller, M. N., Robbins, M. M., Schubert, G., Stoinski, T. S., Viola, B., Watts, D., Wittig, R. M., Wrangham, R. W., Zuberbühler, K., Pääbo, S., & Vigilant, L. (2012). Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proceedings of the National Academy of Sciences, 109, 15716–15721.
Lanham‐New, S. A. (2008). Importance of calcium, vitamin D and vitamin K for osteoporosis prevention and treatment: Symposium on ‘diet and bone health. Proceedings of the Nutrition Society, 67, 163–176.
Lanyon, L. E. (1974). Experimental support for the trajectorial theory of bone structure. Journal of Bone & Joint Surgery, 56B, 160–166.
Latimer, B., & Lovejoy, C. O. (1989). The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality. American Journal of Physical Anthropology, 78, 369–386.
Lazenby, R. A., Skinner, M. M., Hublin, J.‐J., & Boesch, C. (2011). Metacarpal trabecular architecture variation in the chimpanzee (pan troglodytes): Evidence for locomotion and tool‐use? American Journal of Physical Anthropology, 144, 215–225.
Levine, D., Richards, J., & Whittle, M. W. (2014). Whittle's Gait Analysis. Churchill Livingston, Elsevier.
Lloyd, S. (1982). Least squares quantization in PCM. IEEE Transactions on Information Theory, 28, 129–137.
Maga, M., Kappelman, J., Ryan, T. M., & Ketcham, R. A. (2006). Preliminary observations on the calcaneal trabecular microarchitecture of extant large‐bodied hominoids. American Journal of Physical Anthropology, 129, 410–417.
Majumdar, S., Genant, H. K., Grampp, S., Newitt, D. C., Truong, V.‐H., Lin, J. C., & Mathur, A. (1997). Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: In vivo studies in the distal radius using high resolution magnetic resonance imaging. Journal of Bone and Mineral Research, 12, 111–118.
Marchi, D., Harper, C. M., Chirchir, H., & Ruff, C. B. (2019). Relative fibular strength and locomotor behavior in KNM‐WT 15000 and OH 35. Journal of Human Evolution, 131, 48–60.
McNutt, E. J., & DeSilva, J. M. (2020). Evidence for an elongated Achilles tendon in Australopithecus. The Anatomical Record, 303, 2382–2391.
Nozaki, S., Amano, H., Oishi, M., & Ogihara, N. (2021). Morphological differences in the calcaneus among extant great apes investigated by three‐dimensional geometric morphometrics. Scientific Reports, 11, 20889.
Pahr, D. H., & Zysset, P. K. (2009). A comparison of enhanced continuum FE with micro FE models of human vertebral bodies. Journal of Biomechanics, 42, 455–462.
Parfitt, A. M., Travers, R., Rauch, F., & Glorieux, F. H. (2000). Structural and cellular changes during bone growth in healthy children. Bone, 27, 487–494.
Patel, B. A., Ruff, C. B., Simons, E. L. R., & Organ, J. M. (2013). Humeral cross‐sectional shape in suspensory primates and sloths. The Anatomical Record, 296, 545–556.
Pearson, O. M., & Lieberman, D. E. (2004). The aging of Wolff “law”: Ontogeny and responses to mechanical loading in cortical bone. American Journal of Physical Anthropology, 125, 63–99.
Phan, C. M., Matsuura, M., Bauer, J. S., Dunn, T. C., Newitt, D., Lochmueller, E. M., Eckstein, F., Majumadar, S., & Link, T. M. (2006). Trabecular bone structure of the calcaneus: Comparison of MR imaging at 3.0 and 1.5 T with micro‐CT as the standard of reference. Radiology, 239, 488–496.
Prang, T. C. (2015). Calcaneal robusticity in Plio‐Pleistocene hominins: Implications for locomotor diversity and phylogeny. Journal of Human Evolution, 80, 135–146.
Prang, T. C. (2016). The subtalar joint complex of Australopithecus sediba. Journal of Human Evolution, 90, 105–119.
Prang, T. C., & Tocheri, M. W. (2024). Ecological divergence and calcaneal‐cuboid morphology in gorillas. American Journal of Biological Anthropology, 183, e24658.
R Core Team. (2021). R: A language for environment for statistical computing. R Foundation for Statistical Computing. https://R-project.org
Remis, M. J. (1997). Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: Use of variable resources. American Journal of Physical Anthropology, 43, 87–109.
Remis, M. J. (1998a). Feeding Ecology and Positional Behavior of Western Lowland Gorilla (Gorilla gorilla gorilla) in the Central African Republic. (Doctoral Dissertation). Yale University.
Remis, M. J. (1998b). The gorilla paradox: The effects of body size and habitat on the positional behavior of lowland and mountain gorillas. In E. Strasser, J. Fleagle, A. L. Rosenberger, & H. McHenry (Eds.), Primate locomotion (pp. 95–106). Springer.
Remis, M. J. (1999). Tree structure and sex differences in arboreality among western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Primates, 40, 383–396.
Reznikov, N., Liang, H., McKee, M. D., & Piché, N. (2022). Technical note: Mapping of trabecular bone anisotropy and volume fraction in 3D using μCT images of the human calcaneus. American Journal of Biological Anthropology, 177, 566–580. https://doi.org/10.1002/ajpa.24474
Robbins, M. M., & McNeilage, A. (2003). Home range and frugivory patterns of mountain gorillas in Bwindi impenetrable National Park, Uganda. International Journal of Primatology, 24, 467–491.
Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.
Roy, J., Arandjelovic, M., Bradley, B. J., Guschanski, K., Stephens, C. R., Bucknell, D., Cirhuza, H., Kusamba, C., Kyungu, J. C., Smith, V., Robbins, M. M., & Vigilant, L. (2014). Recent divergences and size decreases of eastern gorilla populations. Biology Letters, 10, 20140811.
Rubin, C., Turner, A. S., Bain, S., Mallinckrodt, C., & McLeod, K. (2001). Low mechanical signals strengthen long bones. Nature, 412, 603–604.
Ruff, C. (1988). Hindlimb articular surface allometry in hominoidea and Macaca, with comparisons to diaphyseal scaling. Journal of Human Evolution, 17, 687–714.
Ruff, C., Holt, B., & Trinkaus, E. (2006). Who's afraid of the big bad Wolff?: “Wolff's law” and bone functional adaptation. American Journal of Physical Anthropology, 129, 484–498.
Ruff, C. B., Burgess, M. L., Junno, J.‐A., Mudakikwa, A., Zollikofer, C. P. E., León, M. S. P. d., & McFarlin, S. C. (2018). Phylogenetic and environmental effects on limb bone structure in gorillas. American Journal of Physical Anthropology, 166, 353–372.
Ruff, C. B., Burgess, M. L., Squyres, N., Junno, J.‐A., & Trinkaus, E. (2018). Lower limb articular scaling and body mass estimation in Pliocene and Pleistocene hominins. Journal of Human Evolution, 115, 85–111.
Ruff, C. B., Junno, J.‐A., Burgess, M. L., Canington, S. L., Harper, C., Mudakikwa, A., & McFarlin, S. C. (2022). Body proportions and environmental adaptation in gorillas. American Journal of Biological Anthropology, 177, 501–529.
Ruff, C. B., & Runestad, J. A. (1992). Primate Limb Bone Structural Adaptations. Annual Review of Anthropology, 21, 407–433.
Ruvolo, M. (1996). A new approach to studying modern human origins: Hypothesis testing with coalescence time distributions. Molecular Phylogenetics and Evolution, 5, 202–219.
Ryan, T. M., & Shaw, C. N. (2012). Unique suites of trabecular bone features characterize locomotor behavior in human and non‐human anthropoid primates. PLoS One, 7, e41037.
Ryan, T. M., & Shaw, C. N. (2013). Trabecular bone microstructure scales allometrically in the primate humerus and femur. Proceedings of the Royal Society of London B: Biological Sciences, 280, 20130172.
Sabry, F. F., Ebraheim, N. A., Mehalik, J. N., & Rezcallah, A. T. (2000). Internal architecture of the calcaneus: Implications for calcaneus fractures. Foot & Ankle International, 21, 114–118.
Saers, J. P. P., DeMars, L. J., Stephens, N. B., Jashashvili, T., Carlson, K. J., Gordon, A. D., Shaw, C. N., Ryan, T. M., & Stock, J. T. (2021). Combinations of trabecular and cortical bone properties distinguish various loading modalities between athletes and controls. American Journal of Physical Anthropology, 174(3), 434–450. https://doi.org/10.1002/ajpa.24176
Saers, J. P. P., Gordon, A. D., Ryan, T. M., & Stock, J. T. (2022). Trabecular bone ontogeny tracks neural development and life history among humans and non‐human primates. Proceedings of the National Academy of Sciences, 119(49), e2208772119.
Saers, J. P. P., Ryan, T. M., & Stock, J. T. (2019a). Trabecular bone functional adaptation and sexual dimorphism in the human foot. American Journal of Physical Anthropology, 168(1), 154–169. https://doi.org/10.1002/ajpa.23732
Saers, J. P. P., Ryan, T. M., & Stock, J. T. (2019b). Trabecular bone structure scales allometrically in the foot of four human groups. Journal of Human Evolution, 135, 102654.
Sarringhaus, L. A., Stock, J. T., Marchant, L. F., & McGrew, W. C. (2005). Bilateral asymmetry in the limb bones of the chimpanzee (pan troglodytes). American Journal of Physical Anthropology, 128, 840–845.
Schmitt, D., & Hanna, J. B. (2004). Substrate alters forelimb to hindlimb peak force ratios in primates. Journal of Human Evolution, 46(3), 239–254. https://doi.org/10.1016/j.jhevol.2003.11.008
Schmitt, D., & Larson, S. G. (1995). Heel contact as a function of substrate type and speed in primates. American Journal of Physical Anthropology, 96, 39–50.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675.
Schultz, A. H. (1934). Some distinguishing characters of the mountain gorilla. Journal of Mammalogy, 15, 51–61.
Sokal, R. R., & Rohlf, F. J. (1998). Biometry: The principles and practice of statistics in biological research (3rd ed.). W. H. Freeman and Company.
Sorrentino, R., Carlson, K. J., Figus, C., Pietrobelli, A., Stephens, N. B., DeMars, L. J. D., Saers, J. P. P., Armando, J., Bettuzzi, M., Guarnieri, T., Oxilia, G., Vazzana, A., Parr, W., Turley, K., Morigi, M. P., Stock, J. T., Ryan, T. M., Benazzi, S., Marchi, D., & Belcastro, M. G. (2022). The talar morphology of a hypochondroplasic dwarf: A case study from the Italian late antique period. International Journal of Osteoarchaeology, 32(2), 429–443. https://doi.org/10.1002/oa.3078
Sorrentino, R., Stephens, N. B., Marchi, D., DeMars, L. J. D., Figus, C., Bortolini, E., Badino, F., Saers, J. P. P., Bettuzzi, M., Boschin, F., Capecchi, G., Feletti, F., Guarnieri, T., May, H., Morigi, M. P., Parr, W., Ricci, S., Ronchitelli, A., Stock, J. T., … Benazzi, S. (2021). Unique foot posture in Neanderthals reflects their body mass and high mechanical stress. Journal of Human Evolution, 161, 103093.
Stephens, N. B., Kivell, T. L., Pahr, D. H., Hublin, J.‐J., & Skinner, M. M. (2018). Trabecular bone patterning across the human hand. Journal of Human Evolution, 123, 1–23.
Swartz, S. M., & Biewener, A. A. (1992). Shape and scaling. In A. A. Biewener (Ed.), Biomechanics—Structures and systems: A practical approach (pp. 21–30). Oxford University Press.
Sylvester, A. D., & Terhune, C. E. (2017). Trabecular mapping: Leveraging geometric morphometrics for analyses of trabecular structure. American Journal of Physical Anthropology, 163, 553–569.
Sylvester, A. D., Wescott, D. J., Cunningham, D. L., & Gleiber, D. S. (2023). Effects of obesity on talar micro‐ and macro‐morphology. Journal of Forensic Sciences, 68, 369–381.
Tanck, E., Homminga, J., van Lenthe, G. H., & Huiskes, R. (2001). Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone, 28, 650–654.
Thalmann, O., Fischer, A., Lankester, F., Pääbo, S., & Vigilant, L. (2007). The complex evolutionary history of gorillas: Insights from genomic data. Molecular Biology and Evolution, 24, 146–158.
Tocheri, M. W., Dommain, R., McFarlin, S. C., Burnett, S. E., Troy Case, D., Orr, C. M., Roach, N. T., Villmoare, B., Eriksen, A. B., Kalthoff, D. C., Sench, S., Assefa, Z., Groves, C. P., & Jungers, W. L. (2016). The evolutionary origin and population history of the grauer gorilla. American Journal of Physical Anthropology, 159, 4–18.
Tocheri, M. W., Solhan, C. R., Orr, C. M., Femiani, J., Frohlich, B., Groves, C. P., Harcourt‐Smith, W. E., Richmond, B. G., Shoelson, B., & Jungers, W. L. (2011). Ecological divergence and medial cuneiform morphology in gorillas. Journal of Human Evolution, 60, 171–184.
Tutin, C. E. G., & Fernandez, M. (1985). Foods consumed by sympatric populations of Gorilla g. gorilla and pan t. troglodytes in Gabon: Some preliminary data. International Journal of Primatology, 6, 27–43.
Tutin, C. E. G., & Fernandez, M. (1993). Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lopé reserve, Gabon. American Journal of Primatology, 30, 195–211.
Warton, D. I., Duursma, R. A., Falster, D. S., & Taskinen, S. (2012). Smatr 3– An R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3, 257–259.
Watts, D. P. (1984). Composition and variability of mountain gorilla diets in the central Virungas. American Journal of Primatology, 7, 323–356.
Wolff, J. (1892). The law of bone transformation. Hirschwald.
Xue, Y., Prado‐Martinez, J., Sudmant, P. H., Narasimhan, V., Ayub, Q., Szpak, M., Frandsen, P., Chen, Y., Yngvadottir, B., Cooper, D. N., de Manuel, M., Hernandez‐Rodrigues, J., Lobon, I., Siegismund, H. R., Pagani, L., Quail, M. A., Hvilsom, C., Mudakikwa, Eichler, E. E., Cranfield, M. R., … Scally, A. (2015). Mountain gorilla genomes reveal the impact of long‐term population decline and inbreeding. Science, 348, 242–245.
Yamagiwa, J., Basabose, A. J., Kahekwa, J., Bikaba, D., Ando, C., Matsubara, M., Iwasaki, N., & Sprague, D. S. (2012). Long‐term research on Grauer's gorillas in Kahuzi‐Biega National Park, DRC: Life history, foraging strategies, and ecological differentiation from sympatric chimpanzees. In P. M. Kappeler & D. P. Watts (Eds.), Long‐Term Field Studies of Primates (pp. 385–412). Spring‐Verlag.
Yamagiwa, J., & Mwanza, N. (1994). Day‐journey length and daily diet of solitary male gorillas in lowland and highland habitats. International Journal of Primatology, 15, 207–224.
Yang, Y. (2012). 3D Thin Plate Spine Warping Function. MATLAB central file Exchange.
Zeininger, A., Patel, B. A., Zipfel, B., & Carlson, K. J. (2016). Trabecular architecture in the StW 352 fossil hominin calcaneus. Journal of Human Evolution, 97, 145–158.
Zeininger, A., Schmitt, D., & Wunderlich, R. E. (2020). Mechanics of heel‐strike plantigrady in African apes. Journal of Human Evolution, 145, 102840.
Zelditch, A., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer (2nd ed.). Elsevier Science.
Zioupos, P., & Currey, J. D. (1998). Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone, 22, 57–66.

Auteurs

Christine M Harper (CM)

Department of Biomedical Sciences, Cooper Medical School of Rowan University, Camden, New Jersey, USA.

Biren A Patel (BA)

Department of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
Human and Evolutionary Biology, Department of Biological Sciences, University of Southern California, Los Angeles, California, USA.

Classifications MeSH