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Ontogenetic Variation in the Mandibular Ramus of Great Apes and Humans

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Ontogenetic Variation in the Mandibular Ramus of Great Apes and Humans JOURNAL OF MORPHOLOGY 275:661–677 (2014) Ontogenetic Variation in the Mandibular Ramus of Great Apes and Humans Claire E. Terhune,1* Chris A. Robinson,2 and Terrence B. Ritzman3 1Department of Anthropology, University of Arkansas, Fayetteville, Arkansas 2Department of Biology, Bronx Community College, City University of New York, Bronx, New York 3Institute of Human Origins and School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona ABSTRACT Considerable variation exists in mandib- temporomandibular joint, and the coronoid pro- ular ramus form among primates, particularly great cess, to which the common tendon of the anterior apes and humans. Recent analyses of adult ramal and posterior temporalis muscles is attached. morphology have suggested that features on the Between these two processes is the u-shaped sig- ramus, especially the coronoid process and sigmoid moid notch. The morphology of this region varies notch, can be treated as phylogenetic characters that can be used to reconstruct relationships among great considerably both within and among extant primate ape and fossil hominin taxa. Others have contended taxa. Within the hominids, some authors suggest that ramal morphology is more influenced by function this morphological variation may reflect phylogenetic than phylogeny. In addition, it remains unclear how patterns (Rak et al., 2002, 2007) and/or functional ontogeny of the ramus contributes to adult variation demands of the masticatory apparatus (Hrdlicka, in great apes and humans. Specifically, it is unclear 1940a; Humphrey et al., 1999; Nicholson and Har- whether differences among adults appear early and vati, 2006; Ritzman and Spencer, 2009). However, are maintained throughout ontogeny, or if these differ- the extent to which this morphology varies within ences appear, or are enhanced, during later develop- and among great apes and humans remains rela- ment. To address these questions, the present study tively undocumented and the degree to which ontog- examined a broad ontogenetic sample of great apes and humans using two-dimensional geometric morpho- eny contributes to this shape variation is unclear. metric analysis. Variation within and among species This study seeks to examine mandibular ramus was summarized using principal component and thin form throughout ontogeny in the great apes and plate spline analyses, and Procrustes distances and humans, with the ultimate goal of addressing these discriminant function analyses were used to statisti- potentially conflicting conclusions regarding the util- cally compare species and age classes. Results suggest ity of mandibular ramal morphology for understand- that morphological differences among species in ramal ing phylogenetic relationships and/or functional morphology appear early in ontogeny and persist into variation within fossil and extant hominids. adulthood. Morphological differences among adults are particularly pronounced in the height and angulation Previous Morphological Descriptions of the of the coronoid process, the depth and anteroposterior Mandibular Ramus length of the sigmoid notch, and the inclination of the ramus. In all taxa, the ascending ramus of the young- The majority of previous work describing the est specimens is more posteriorly inclined in relation mandibular ramus in extant hominids has focused to the occlusal plane, shifting to become more upright on intraspecific human variation (e.g., Hrdlicka, in adults. These results suggest that, although there 1940a, b, c; Humphrey et al., 1999; Nicholson and are likely functional influences over the form of the Harvati, 2006). Aitchison (1965) qualitatively coronoid process and ramus, the morphology of this observed that chimpanzees possess a coronoid region can be profitably used to differentiate among great apes, modern humans, and fossil hominid taxa. J. Morphol. 275:661–677, 2014. VC 2014 Wiley Periodicals, Inc. Additional Supporting Information may be found in the online ver- sion of this article. KEY WORDS: primate ontogeny; mandibular shape; *Correspondence to: Claire E. Terhune, Department of Anthropol- geometric morphometrics ogy, University of Arkansas, Fayetteville, AR 72701. E-mail: [email protected] INTRODUCTION Received 7 August 2013; Revised 7 December 2013; In all primates, and more generally across mam- Accepted 15 December 2013. mals, the ramus of the mandible terminates supe- Published online 1 February 2014 in riorly in two processes: the condylar process, Wiley Online Library (wileyonlinelibrary.com). which forms the mandibular component of the DOI 10.1002/jmor.20246 VC 2014 WILEY PERIODICALS, INC. 662 C.E. TERHUNE ET AL. process that is higher than those of gorillas and Given these analyses, Rak et al. (2002, 2007) sug- orangutans, which he related to the more oblique gested that aspects of ramus form, especially the angle that the chimpanzee ramus made with the shape of the coronoid process and sigmoid notch, alveolar margin. In addition, he argued that great may be useful characters for reconstructing phylo- ape species could be clearly differentiated from genetic relationships among great ape and fossil each other in the height of the ramus above the hominin taxa. Rak et al. (2007) argued that the occlusal plane, with Gorilla having the tallest utility of these features for phylogenetic analyses is ramus and Pan the shortest. This observation was strengthened by their finding that variation in supported by the work of Humphrey et al. (1999), these features is not related to the size and orienta- who documented that the height of the mandibu- tion of the temporalis. The basis of this argument lar ramus relative to the occlusal plane is lowest rests primarily on the observation that, while chim- in humans and highest in Gorilla. They also found panzee and gorilla males and females differ in cra- that humans exhibit a relatively greater distance nial cresting patterns (which largely reflect the between the coronoid and condyle (i.e., a wider sig- orientation of the temporalis), males and females of moid notch) than great apes. these species do not differ in ramal morphology Rak et al. (2002, 2007) recently performed a (Rak et al., 2007). In addition, they suggested that detailed analysis of ramal morphology in fossil hom- because Au. afarensis has been reconstructed as inins and extant hominids, with a particular focus being dissimilar to Gorilla in its dietary behavior on the shape of the sigmoid notch. In a dimensional and habitat, early hominin taxa and gorillas were (2D) analysis of ramal morphology, including the unlikely to have evolved these shared features coronoid and condylar processes, Rak et al. (2002) because of adaptations to a similar dietary niche. identified different morphologies in Neanderthals Given these results, they argued that Au. afarensis and modern humans. Specifically, these authors and P. robustus (and Au. africanus as well, based demonstrated that Neanderthals possess a rela- on the preserved morphology of Sts 7) shared these tively lower condylar process (and correspondingly characters as synapomorphies and that these syna- higher coronoid process), and a sigmoid notch with pomorphies unite these species in a clade, casting the deepest point situated closer to the condyle. doubt on claims that Au. afarensis was basal to all These researchers linked this unique morphology to later hominin species. Based on these traits, Rak a “profound specialization of the masticatory sys- et al. (2007) proposed instead that this clade was tem” in this taxon (Rak et al., 2002: 202), which part of a side branch of hominins that did not con- they suggested may be linked to increased maxi- tribute to the ancestry of the genus Homo. mum jaw gape in Neanderthals compared to mod- Other researchers have argued that mandibular ern humans. Other studies comparing three- characters are generally poor indicators of taxonomic dimensional (3D) landmark configurations in mod- identity and phylogenetic relationships, primarily ern humans and Neanderthals similarly described duetothehighstrainsexperiencedbythemandible Neanderthals as having an “asymmetrical” sigmoid that may result in increased phenotypic plasticity notch and a coronoid that is taller than the condyle (Wood and Lieberman, 2001; Schmittbuhl et al., (Nicholson and Harvati, 2006; Harvati et al., 2011). 2007) and greater potential for homoplasy (e.g., However, these authors found little support for the Skelton and McHenry, 1992; Turner and Wood, argument that the unique mandibular morphology 1993; Begun, 1994; McHenry, 1994; Lieberman of Neanderthals was related to mechanical demands et al., 1996; Asfaw et al., 1999). In contrast, some placed on the mandible. studies have found that homoplasy in characters Rak et al. (2007) further documented the 2D- related to mastication is no greater than in charac- shape of the margin of the anterior ramus (i.e., the ters from other regions of the skull (Collard and coronoid process) and the sigmoid notch in great Wood, 2001), and others suggested that including apes and humans. Using these data, they were able characters under high masticatory strain increases to assign specimens to the correct taxon with the accuracy of taxonomic analyses (Collard and approximately 82% accuracy, and they identified a Lycett, 2009). Furthermore, other researchers have set of traits unique to Gorilla relative to modern found that variation among Gorilla and Pan subspe- humans, chimpanzees, and orangutans. These cies in mandibular metrics is less than one would traits
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