Hominoid Arcade Shape: Pattern and Magnitude of Covariation
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Journal of Human Evolution 107 (2017) 71e85 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol Hominoid arcade shape: Pattern and magnitude of covariation * Stefanie Stelzer a, , Philipp Gunz a, Simon Neubauer a, Fred Spoor a, b a Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany b Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK article info abstract Article history: The shape of the dental arcade and canine size distinguish extant humans from all apes. Humans are Received 8 October 2015 characterized by a parabolic arcade with short postcanine tooth rows and small canines, whereas apes Accepted 28 February 2017 have long, U-shaped arcades with large canines. The evolutionary and biomechanical mechanisms un- derlying arcade shape differences between and within groups are not well understood. It is unclear, for example, whether evolutionary changes in the covariation among modules comprising the upper and Keywords: lower jaws are the cause and/or consequence of different arcade shapes. Here we use 3D geometric Maxilla morphometric methods to explore to what extent the morphological differences in arcade shape be- Mandible Premaxilla tween living hominoids are related to differences in covariation of upper and lower jaws, and the pre- Integration maxilla and the maxilla. We show that all extant hominoids follow a very similar covariation pattern Jaw between upper and lower dental arcades, as well as between the premaxilla and the maxilla. We find Canine comparably high magnitudes of covariation between the premaxilla and the maxilla in all groups. Be- tween the upper and lower jaws, levels of covariation are similar in apes (Pan, Gorilla, Pongo, and Hylobates), but overall lower in extant humans. Our results demonstrate an independence of the pattern of arcade shape covariation from dental spatial arrangements. Importantly, we show that a shared hominoid pattern of covariation between premaxilla and maxilla together with the covariation of upper and lower jaw is consistent with major evolutionary arcade shape changes in hominoids. We suggest that with the reduction of canine and diastema size in hominins, the incisors move posteriorly and the tooth row becomes more parabolic. Our study provides a framework for addressing questions about fossil hominin dentognathic diversity, including inter- and intraspecific variation and associations of upper and lower jaw morphology. © 2017 Elsevier Ltd. All rights reserved. 1. Introduction 1942), where canine size can vary strongly inter- and intraspecifi- cally (Almquist, 1974; Leutenegger and Kelly, 1977; Oxnard et al., Dentognathic morphology of extant humans and apes differs 1985; Leutenegger and Shell, 1987; Plavcan and van Schaik, 1992; notably in canine size and arcade shape. In apes, the arcades are U- Plavcan, 1993; Kelley, 1995). shaped with narrow and near-parallel postcanine tooth rows. Modern human dental arcades are usually referred to as being Furthermore, dental arcade shape varies within and between ape parabolic (Angle, 1899; Broomell, 1902; Le Gros Clark, 1950; Genet- species: posteriorly diverging or converging postcanine tooth rows Varcin, 1969), elliptic (Black, 1902; Garn, 1968; Currier, 1969; result in a range of arcade contours (Hellman, 1919). In some in- Brader, 1972) or catenary (MacConaill and Scher, 1949; Scott, dividuals the arcade tapers in the premolar region to diverge again 1957; Engel, 1979), with upper and lower arcades having slightly more posteriorly, giving it a saddle shape (Hellman, 1919; Remane, different shapes (Hellman, 1919; Engel, 1979). Incisors and canines 1921). The large lower canines are accommodated in a diastema are of almost equal size (Schwartz, 1995) and their occlusal surfaces between the upper lateral incisor and the enlarged upper canine; in are on the same level as the postcanine dentition. the mandible, the upper canine is accommodated between the Intra- and interspecific differences in cranial and mandibular lower canine and the lower premolars (Angle, 1899; Hellman, architecture among primates have been related to differences in masticatory behavior, including varying mechanical stress (Hrdlicka, 1940; Hylander, 1972, 1979; Carlson and Vangerven, 1977; Weijs and Hillen, 1984; Bouvier, 1986; Weijs and Hillen, * Corresponding author. E-mail address: [email protected] (S. Stelzer). 1986; Armelagos et al., 1989; Ravosa, 1990; Corruccini, 1991; http://dx.doi.org/10.1016/j.jhevol.2017.02.010 0047-2484/© 2017 Elsevier Ltd. All rights reserved. 72 S. Stelzer et al. / Journal of Human Evolution 107 (2017) 71e85 Herring, 1993; Anapol and Lee, 1994; Larsen, 1995; Cassidy et al., Lieberman et al., 2000; Marroig and Cheverud, 2001; Ackermann, 1998; Sardi et al., 2004; Lieberman, 2008; von Cramon-Taubadel, 2002; Gonzalez-Jose et al., 2004; Marroig et al., 2004; Acker- 2011; Prasad et al., 2013). These biomechanical arguments mann, 2005; Goswami, 2006; Gunz and Harvati, 2007; Mitter- emphasize that relative position and length of the dental arcade oecker and Bookstein, 2008; Porto et al., 2009; Makedonska et al., influence the stress distribution (Witzel and Preuschoft, 2002). In 2012; Villmoare et al., 2014). In this study we assess (1) whether the this view, phenotypic variation of the upper and lower jaw is seen same applies to hominoid upper and lower dental arcades, or (2) as a consequence rather than a precondition for different force whether the variation in extant arcade shapes is associated with a distributions. In apes relatively long tooth rows and prognathic variation of the underlying patterns of covariation. dental arcades seem to be biomechanically advantageous, whereas The magnitude of covariation has been related to material in humans the parabolic arcade is seen as a side effect of reduction properties of food, in that taxa relying on a mechanically chal- in bite- and chewing forces and the reorganization of the face lenging diet have stronger integrated upper and lower jaws (Preuschoft, 1989; Witzel and Preuschoft, 1999) with little biome- (Marroig and Cheverud, 2001; Makedonska et al., 2012). Pan, Pongo, chanical significance (Preuschoft and Witzel, 2004). Recent studies Gorilla, and Hylobates consume different proportions of leaves, fruit, in capuchin monkeys (Makedonska et al., 2012) and modern other plant parts, or insects, and their dietary preferences are humans (Noback and Harvati, 2015) showed that, at least within dependent on season, food availability, habitat and sex. In general, groups, dental arcade shape (in contrast to size and position) is however, Pan, Pongo, and Hylobates are more frugivorous, whereas largely independent from masticatory forces. These authors found Gorilla is more reliant on leaves (MacKinnon, 1974; Rijksen, 1978; correlations between diet and shape of the temporalis muscle and Gittins and Raemaekers, 1980; Watts, 1984; Galdikas, 1988; Tutin the cranium, but none between subsistence and maxillary arch and Fernandez, 1993; Knott, 1998; McConkey et al., 2003; Rogers shape. et al., 2004; Boesch et al., 2006; Doran-Sheehy et al., 2009). The evolutionary and biomechanical mechanisms underlying Morphologically, this difference is reflected in relative dental sizes. the differences in arcade shape between extant humans and apes, Frugivores have relatively larger incisors, while foliovores have as well as those underlying the within-group variability, are not relatively larger molars (Hylander, 1975; Kay and Hylander, 1978). well understood. The evolutionary trajectory of our lineage is In comparison to apes, modern humans have a more generalist diet, interesting in this regard, as arcade shape varies considerably where extra-oral food processing via tool use or cooking is thought among fossil hominins (e.g., Weidenreich, 1936; Tobias, 1967; to have reduced the masticatory effort since the emergence of our Johanson et al., 1978; Johanson and White, 1979; Greenfield, species or even earlier (e.g. Brace et al., 1987; Wrangham et al., 1992). Besides a general reduction in absolute canine size, early 1999; Richards et al., 2001; Teaford et al., 2002; Henry, 2010). hominins like Australopithecus anamensis and Australopithecus While a correlation with diet seems likely, some authors have afarensis possess primitive features such as a small diastema be- suggested that the lower covariation magnitudes in the human tween the upper incisor and the canine, as well as parallel to cranium (Marroig et al., 2009; Porto et al., 2009) and pelvis slightly diverging tooth rows (Schwartz, 1995; White et al., 2000; (Grabowski et al., 2011) may indicate a general relaxation of inte- Ward et al., 2001; Kimbel and Delezene, 2009). Some early Homo gration in the hominin lineage. These authors argued that the specimens retain long and almost parallel tooth rows, whereas change in magnitude of integration might have paved the way for others have shorter postcanine rows and non-projecting frontal the development of the morphological changes characterizing our tooth rows (Tobias, 1991; Wood, 1991; Rightmire, 1993; Kimbel lineage. In addition to the two aforementioned aims, we therefore et al., 1997; Clarke, 2012; Leakey et al., 2012; Spoor et al., 2015). also assess (3) whether there are differences in the magnitude of Large-scale differences in jaw shapes have been used to support covariation between the groups, and (4) whether there are differ- arguments