AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:519–530 (2010) An Interspeciﬁc Analysis of Relative Jaw-Joint Height in Primates Brooke A. Armﬁeld1,2* and Christopher J. Vinyard1,2 1 Department of Anatomy and Neurobiology, Northeastern Ohio Universities College of Medicine (NEOUCOM), Rootstown, OH 44272 2 Skeletal Biology Research Focus Area, NEOUCOM, Rootstown, OH 44272 KEY WORDS posterior facial height; basicranial ﬂexion; facial kyphosis; craniofacial growth ABSTRACT Jaw-joint height (JJH) above the occlusal plane is thought to be inﬂuenced by cranial base angle (CBA) and facial angulation during growth. To better understand how JJH relates to midline craniofacial form, we test the hypothesis that relative increases in JJH are correlated with increasing CBA ﬂexion and facial kyphosis (i.e., ventral bending) across primates. We compared JJH above the occlusal plane to CBA and the angle of facial kyphosis (AFK) across adults from 82 species. JJH scales with positive allometry relative to a skull geometric mean in anthropoids and most likely strepsirrhines. Anthropoid regressions for JJH are elevated above strepsirrhines, whereas catarrhines exhibit a higher slope than platyrrhines. Semipartial correlations between relative JJH and both CBA and AFK show no association across a small strepsirrhine sample, limited associations among catarrhines and anthropoids, but strong correlations in platyrrhines. Contrary to our hypothesis, however, increases in relative JJH are correlated with relatively less ﬂexed basicrania and more airorhynch faces (i.e., reduced ventral bending) in platyrrhines. The mosaic pattern of relationships involving JJH across primate clades points to multiple inﬂuences on JJH across primates. In clades showing little association with basicranial and facial angles, such as strepsirrhines, the potential morphological independence of JJH may facilitate a relative freedom for evolutionary changes related to masticatory function. Finally, failure to associate relative JJH and basicranial ﬂexion in most clades suggests that the relatively taller JJH and more ﬂexed basicrania of anthropoids compared to strepsirrhines may have evolved as an isolated event during the origin of anthropoids. Am J Phys Anthropol 142:519– 530, 2010. V 2010 Wiley-Liss, Inc. The height of the jaw joint above the occlusal plane (JJH) is hypothesized to be functionally and/or developmentally integrated with other craniofacial regions including components of both the neurocranium and facial skull. These hypotheses center on two concepts: (1) there is a functional component to selection for taller JJH enhancing masticatory performance and/or (2) there is a growth relationship between the cranial base and face that inﬂuences the height of the jaw joint. Functional hypotheses concentrate on the implications of JJH for masticatory mechanics related to maximum jaw opening and/or bite force (e.g., Biegert, 1963; Zingeser, 1973; Greaves, 1974, 1980, 1995; Herring and Herring, 1974; Ward and Molnar, 1980; Osborn, 1987; Ravosa et al., 2000; Williams et al., 2002; Vinyard et al., 2003). Alternatively, growth- and development-related hypotheses focus on how posterior facial height is inﬂuenced by changes in basicranial and/or upper facial morphology (e.g., Enlow and Hunter, 1968; McCollum, 1997, 1999; McCarthy, 2001; Sondang et al., 2003; Bastir and Rosas, 2004, 2005, 2006). For example, the relatively taller JJH of living anthropoids compared to strepsirrhines has been explained by Ravosa et al. (2000) as related to increased ﬂexion of the anthropoid cranial base and concomitant changes in facial kyphosis. Although growth-related inﬂuences on posterior facial height have been studied in humans and other apes (Enlow and Hunter, 1968; Enlow, 1990; Bastir and Rosas, 2004, 2005, 2006), we lack a primate-wide analysis of associations between JJH, cranial base angulation (CBA), and angle of facial kyphosis (AFK). By exploring these relationships across primate clades, we hope to better understand how evolutionary changes in cranial base and facial regions might inﬂuence JJH variation across primates [see Lieberman et al. (2000)]. These results may also help identify instances where changes in craniofacial form that are unrelated to the masticatory apparatus have an effect on masticatory function (Ravosa et al., 2000; Bastir and Rosas, 2005). C 2010 V WILEY-LISS, INC. C Cranial base and facial growth-related inﬂuences on JJH The growth and form of the cranial base, particularly, the angle formed between anterior and posterior basicranial segments, is argued to play an important role in determining primate skull form (e.g., Lieberman et al., 2000 and references therein). Increasing relative brain size across primates, is widely hypothesized to result in Grant sponsors: Sigma-Xi, Boise Fund, AMNH, NSF; Grant numbers: SBR-9701425, BCS-0094666; Grant sponsor: L.S.B. Leakey Foundation. *Correspondence to: Brooke A. Armﬁeld, Department of Anatomy and Neurobiology—NEOUCOM, 4209 St. Rt. 44, Box 95, Rootstown, OH 44272. E-mail: firstname.lastname@example.org Received 24 May 2009; accepted 10 November 2009 DOI 10.1002/ajpa.21251 Published online 1 February 2010 in Wiley InterScience (www.interscience.wiley.com). 520 B.A. ARMFIELD AND C.J. VINYARD Fig. 1. Diagram depicting a general hypothesized set of relationships among craniofacial elements examined here (see text for more details). In anthropoids, increases in brain size relative to basicranial length are hypothesized to cause increased basicranial ﬂexion (1). A more ﬂexed cranial base angle is hypothesized to inﬂuence orbital orientation, facial kyphosis (2), and posterior facial height (i.e., jaw-joint height, JJH) (3). Increased facial kyphosis may also correlate with increased JJH (4). Finally, changes in JJH have functional consequences for masticatory apparatus performance related to biting, chewing, and jaw-opening (5). Additional linkages (including bi-directional linkages) have been suggested, but are omitted for simplicity. a more ﬂexed cranial base to accommodate an enlarged brain (Moss, 1958; DuBrul and Laskins, 1961; Biegert, 1963; Vogel, 1968; Ross and Ravosa, 1993; Ross and Henneberg, 1995; Ross, 1996; Spoor, 1997; Lieberman et al., 2000; Ross et al., 2004) (Fig. 1). Tests of this spatial packing hypothesis yield signiﬁcant association between relative adult brain size and CBA across several primate clades (e.g., Ross and Ravosa, 1993; Ross et al., 2004).1 Additionally, the morphology of the cranial base is hypothesized to inﬂuence upper and mid-facial form (Dabelow, 1929, 1931; Enlow and Hunter, 1968; Enlow and McNamara, 1973; Enlow, 1990; Ross and Ravosa, 1993; Spoor, 1997; Lieberman et al., 2000, 2008; Ravosa et al., 2000; McCarthy and Lieberman, 2001; Bastir and Rosas, 2004, 2005, 2006; Bastir et al., 2004; Kuroe et al., 2004).2 Basic support for this observation follows from the facts that (1) basicranial growth largely precedes facial growth and (2) the face develops around the basicranium with signiﬁcant interactions occurring during growth at speciﬁc structural connections between these regions [i.e., the growth counterparts deﬁned by Enlow (Enlow and Hunter, 1968; Enlow et al., 1969, 1971; Enlow and McNamara, 1973; Enlow and Azuma, 1975; Enlow, 1990]. Previous interspeciﬁc studies of anthropoids suggest that as a result of the integration between the cranial base and face, an increase in basicranial ﬂexion results in downward rotation of the orbits and posterior face (Ross and Ravosa, 1993; Ross and Henneberg, 1995; McCarthy, 2001; McCarthy and Lieberman, 2001) (Fig. 1). The subsequent result is an increase in facial kyphosis (i.e., the angular relationship of the face and cranial vault) with increasing cranial base ﬂexion (DuBrul and Laskin, 1961; Biegert, 1963; Enlow and Azuma, 1975; Ross and Ravosa, 1993; Lieberman et al., 2000; McCarthy and Lieberman, 2001) (Fig. 1). Increasing facial kyphosis is therefore hypothesized to increase JJH given that downward rotation of the toothrow contrasted with a relatively stationary glenoid fossa may increase the vertical distance from the occlusal plane to the glenoid fossa (Ravosa et al., 2000). Based on the observed correlations between facial orientation and cranial base ﬂexion in anthropoids and JJH differences between strepsirrhines and anthropoids, Ravosa et al. (2000, p 509) hypothesized that variation in jaw-joint height is linked to suborder differences in relative facial height due in turn to increased encephalization, basicranial ﬂexion, and facial kyphosis in anthropoids (Fig. 1). We conduct an interspeciﬁc analysis of JJH, CBA, and AFK to assess whether variation in relative JJH across primates is potentially associated with variation in these craniofacial components. We develop two predictions building on the Ravosa et al.’s (2000) hypothesis. Prediction One suggests that relative JJH will increase with greater ﬂexion in CBA. Prediction Two suggests that relative JJH will increase with increasing ﬂexion in AFK. Furthermore, we examine allometric variation in these dimensions and compare these scaling patterns between primate suborders and anthropoid infraorders. Allometric differences in JJH among these clades may provide important insight into evolutionary changes in masticatory function that occurred with the rise of these higher-order primate clades (Ravosa et al., 2000). 1 It is important to note that signiﬁcant interspeciﬁc correlations between relative brain size and ﬂexion are not necessarily replicated within primate species during ontogeny (Bjork, 1955; Jeffery and Spoor, 2002, 2004; Jeffery, 2003). During certain periods of ontogeny, an association is not evident or can even be reversed (i.e., cranial base extension with increasing brain size) indicating the multifactorial nature of primate cranial base growth (Sirianni and Swindler, 1979; Lieberman et al., 2000; Jeffery, 2003). 2 We want to clarify that we are not excluding facial growth from inﬂuencing basicranial form during early ontogeny (Lieberman et al., 2000, 2008; Jeffrey and Spoor, 2002; Bastir and Rosas, 2006; Bastir et al., 2006), but rather focusing on one aspect of a multifactorial relationship. Our correlational analysis cannot discriminate cause and effect in any observed association between various cranial components. American Journal of Physical Anthropology MATERIALS AND METHODS Samples and measurements We collected data from 82 adult primate species including 39 strepsirrhines, 17 platyrrhines, and 26 catarrhines (Appendix A). Typically, species means were based on three to ﬁve adult males and females, respectively. Because we compiled data from literature sources, the number of individuals per species varies across dimensions and species means reﬂect measurements taken on different individuals. We deﬁne JJH as the vertical distance from the maxillary occlusal plane to the glenoid articular surface perpendicular to this occlusal plane (Biegert, 1963) 521 JJH ACROSS PRIMATES Fig. 2. Measures of (a) jaw-joint height (Vinyard, 1999), (b) cranial base angle (Lieberman and McCarthy, 1999), and facial kyphosis (Ross and Ravosa, 1993). (Fig. 2a). The maxillary occlusal plane is deﬁned by a straight line passing through the tips of the anterior maxillary premolar and the posterior cusp of the last maxillary molar. Similar to the posterior facial height measurement of Bastir and Rosas (2004), JJH attempts to capture the vertical height of the posterior face. We measured JJH from lateral-view video captures using SigmaScan Pro 4.0 software (SPAA, Inc.). CBA and AFK angles were taken from data provided in Lieberman et al. (2000) based on lateral-view radiographs (Fig. 2b). We adopted the angle from basion-sellaforamen caecum as an estimate of basicranial angulation (Lieberman and McCarthy, 1999). We used this estimate of basicranial angulation, because the distance from sella to foramen caecum only captures variation in the anterior cranial ﬂoor, and this distance contributes to growth counterparts related to both the upper and mid-face (Enlow, 1990; Spoor, 1997; Lieberman and McCarthy, 1999). Facial kyphosis is estimated as the angle formed by the intersection of the planes of the clivus and the ﬂoor of the nasal fossa (Hofer, 1952; Ross and Ravosa, 1993; Lieberman et al., 2000). Ten additional skull measurements were collected and used to generate a geometric mean (GM) for estimating overall skull size. Species means are provided in Appendix A. Analyses Linear measurements were natural log transformed before analysis to improve linearity and reduce sizerelated heteroscedascity. Given our broad interspeciﬁc sampling, size differences across primate species repre- sent a key intervening factor potentially inﬂuencing relationships among these craniofacial dimensions. Because our goal is to examine structural relationships between skull elements, we used a GM of several skull measurements (Appendix A) to estimate overall skull size (Vinyard, 2008). We examined scaling patterns for JJH, CBA, and AFK relative to this cranial size estimate using least squares (LS) and reduced major axes (RMA) regressions. We calculated the RMA 95% conﬁdence interval using the LS conﬁdence interval (Sokal and Rohlf, 1995). Scaling patterns were examined in both suborders and separately for platyrrhines and catarrhines. We used analyses of covariance (ANCOVA) relative to the skull GM to compare scaling patterns for JJH and CBA between suborders and the two anthropoid infraorders. We used ANOVA to compare AFK among these groups as AFK was not correlated with the skull GM. To test Predictions One and Two from Ravosa et al. (2000), we calculated semipartial product-moment correlations between relative JJH and both CBA and AFK. In these semipartial correlations, relative JJH is estimated as the residuals from a LS regression of JJH on the skull GM across our entire primate sample.3 Because primates differ in their phylogenetic relatedness, we performed analyses using independent contrasts (ICs) in addition to conventional statistical tests. Phylogenies were taken from Smith and Cheverud (2002) and Purvis (1995) for anthropoids and Vinyard and Hanna (2005) for strepsirrhines (Appendix B). ICs were performed using Compare 4.6 (Martins, 2004). Branch lengths were set to unity to eliminate bias due to arbitrary assignments of branch lengths for primate taxa (Garland et al., 1992; Diaz-Uriarte and Garland, 1998). From contrast data, we estimated regressions and correlations as outlined earlier. We performed phylogenetic ANCOVAs and ANOVAs by suborder and anthropoid infraorder following Garland et al. (1993) using the PDSimul, PDSingle, and PDANOVA modules in PDAP. We applied a sequential Bonferroni adjustment (a 5 0.05) due to the multiple comparisons in the regression, ANCOVA, and ANOVA analyses (Rice, 1989). RESULTS Scaling patterns among primate clades JJH among strepsirrhines shows a nonsigniﬁcant or moderate correlation with skull size for the IC and conventional data, respectively (Table 1). These low correlations underlie a mixed scaling pattern where conventional and IC LS regressions suggest negative allometry, although not excluding isometry, while the conventional and IC RMA regressions suggest positive allometry (Table 1, Fig. 3a). Among anthropoids, JJH scales with strong positive allometry relative to skull size (Table 1, Fig. 3a) [see also Ravosa et al. (2000)]. Similarly, JJH 3 Previous critiques of using residuals and ratios in size adjustment (e.g., Corruccini, 1987; Jungers et al., 1995; Smith, 2005) illustrate the importance of proper interpretation of results from these different size-adjustment approaches. In this case, we came to similar conclusions when repeating the analysis using dimensionless shape ratios relative to the skull geometric mean. Additionally, we came to qualitatively similar conclusions when examining semipartial correlations calculated from clade-speciﬁc samples rather than the primate-wide sample. American Journal of Physical Anthropology Nc 37 42 16 26 11 28 10 18 11 29 10 19 Cladeb Strep Anth Plat Cat Strep Anth Plat Cat Strep Anth Plat Cat (60.61) (60.35) (60.63) (60.43) – – – 210.38 (611.13) – – 24.56 (621.48) – 0.70 1.73 2.28 1.36 IC LS sloped,e (60.61) (60.35) (60.63) (60.43) – – – 215.95 (611.13) – – 36.01 (621.48) – 1.91 2.05 2.53 1.69 IC RMA sloped,e 0.37 0.85 0.90 0.80 20.01 20.25 0.45 20.65 0.37 20.07 0.68 20.23 (0.026) (\0.001) (\0.001) (\0.001) (0.99) (0.21) (0.19) (0.003) (0.27) (0.73) (0.03) (0.34) IC rf (60.40) (60.21) (60.45) (60.28) – 27.10 (65.63) 2 9.42 (68.15) 28.40 (66.40) – – 21.71 (618.36) – 0.88 1.79 2.23 1.71 LS slopee,g 81.35 190.72 139.15 193.63 21.41 24.07 25.47 23.84 (61.26) (60.78) (61.54) (61.09) – (621.12) (627.58) (625.23) – – (662.08) – LS constantg 1.46 (60.40) 1.90 (60.21) 2.37 (60.45) 1.84 (60.28) – 215.68 (65.63) 2 13.75 (68.15) 214.70 (66.40) – – 31.29 (618.36) – RMA slopee,g 291.58 222.65 218.40 124.59 23.10 24.51 25.93 24.33 (61.26) (60.78) (61.54) (61.09) – (621.12) (627.58) (625.23) – – (662.08) – RMA constantg 0.60 0.94 0.94 0.93 20.15 20.45 0.69 20.57 0.44 20.05 0.69 20.26 (\0.001) (\0.001) (\0.001) (\0.001) (0.66) (0.015) (0.029) (0.013) (0.18) (0.79) (0.026) (0.29) rh b JJH, jaw-joint height (mm); CBA, cranial base angle (degrees); AFK, facial kyphosis angle (degrees). Strep, strepsirrhines; Anth, anthropoids; Plat, platyrrhines; Cat, catarrhines. c N, sample size for each clade. d IC LS slope refers to the least-squares slope estimate (passing through the origin) based on independent contrasts (IC). IC RMA slope refers to the reduced major axis slope estimate based on contrast data. The 95% conﬁdence intervals (CI) for the slope are provided in parentheses. e For JJH, italicized values denote positive allometry. Values in normal font indicate that the slope does not differ signiﬁcantly from isometry. f IC r refers to the product-moment correlation based on independent contrasts. P values are provided in parentheses. Bold values are signiﬁcant after Bonferroni adjustment at a \ 0.05. g LS slope refers to the least-squares regression slope. LS constant refers to the least-squares constant. RMA slope refers to the reduced major axis slope. RMA constant refers to the reduced major-axis constant. The 95% conﬁdence intervals (CI) for the slope and constant are provided in parentheses. h r refers to the product-moment correlation. P-values are provided in parentheses. Bold values are signiﬁcant after Bonferroni adjustment at a \ 0.05. a AFK CBA JJH Dimensiona TABLE 1. Scaling patterns for ln jaw-joint height (JJH), cranial base angle (CBA), and the angle of facial kyphosis (AFK) versus the ln skull GM for different primate clades 522 B.A. ARMFIELD AND C.J. VINYARD American Journal of Physical Anthropology Fig. 3. Plot of (a) ln jaw-joint height, (b) cranial base angle, and (c) facial kyphosis on ln skull geometric mean (symbols: l, Strepsirrhines; n, Platyrrhines; ~, Catarrhines). scales with positive allometry in both anthropoid infraorders, although the 95% CI for the IC LS slope in catarrhines includes a possible isometric scaling pattern. Among strepsirrhines, angular changes in the basicranium (CBA) and AFK are not correlated with skull size 523 JJH ACROSS PRIMATES a TABLE 2. ANCOVA and ANOVA comparisons between primate clades IC ANCOVAc Dimension b N Slope Anthropoids versus Strepsirrhines JJH 42/37 Anth [ Strep (P 5 0.02) CBA 11/28 NS 10/18 NS AFK 10/19 – Constant Slope Constant IC ANOVAe ANOVAf – Anth [ Strep (P \ 0.001) NS – – – NS – – – – NS NS Cat [ Plat (P 5 0.035) Plat [ Cat (P 5 0.001) – – – – – – – – NS NS Strep [ Anth (P 5 0.02) – AFK 11/29 – Platyrrhines versus Catarrhines JJH 16/26 NS CBA ANCOVAd NS Plat [ Cat (P 5 0.008) – See Table 1 for abbreviations. Bold values are signiﬁcant (a \ 0.05) after Bonferroni adjustment. Anthropoid sample sizes are listed ﬁrst followed by strepsirrhine sample sizes. Similarly, platyrrhines are listed ﬁrst followed by catarrhines. c IC ANCOVA of clade differences in regression slopes and constants for ln JJH and cranial angles relative to the ln skull GM are based on a simulated F-statistic incorporating phylogenetic nonindependence (Garland et al., 1993); NS indicates no signiﬁcant difference in slope or constant between infraorders (a 5 0.05). d ANCOVA of LS regressions for ln JJH and cranial angles relative to the ln skull GM between primate clades. e IC ANOVA of clade differences in AFK are based on a simulated F-statistic incorporating phylogenetic non-independence (Garland et al., 1993). f ANOVA between primate clades for AFK. a b TABLE 3. Correlations and semipartial correlations among relative ln jaw-joint height (JJH), cranial base angle (CBA), and the angle of facial kyphosis (AFK)a Strepsirrhines Relative ln JJHb—CBA Relative ln JJH—AFK CBA—AFK Anthropoids Catarrhines Platyrrhines r IC r rc IC r r IC r r IC r 20.08 (P 5 0.82) 20.28 (P 5 0.40) 0.131 (P 5 0.72) 0.23 (P 5 0.52) 0.35 (P 5 0.32) 20.12 (P 5 0.77) 0.41 (P 5 0.03) 0.38 (P 5 0.04) 0.44 (P 5 0.02) 0.52 (P 5 0.005) 0.32 (P 5 0.10) 0.34 (P 5 0.08) 0.20 (P 5 0.43) 20.01 (P 5 0.96) 0.19 (P 5 0.45) 0.09 (P 5 0.73) 20.09 (P 5 0.73) 0.24 (P 5 0.35) 0.85 (P 5 0.002) 0.85 (P 5 0.002) 0.78 (P 5 0.005) 0.73 (P 5 0.03) 0.60 (P 5 0.09) 0.53 (P 5 0.12) a See Table 1 for abbreviations. Relative ln JJH takes the skull GM into account in the semipartial correlation. Relative ln JJH values are equivalent to the residuals from a least-squares regression of ln JJH on the ln skull GM across the entire primate sample. c Bold values are signiﬁcant (a \ 0.05). b (Table 1, Fig. 3). Although the lack of a strong association may be related to the small strepsirrhine sample sizes, these results follow previous observations that these angular dimensions do not strongly covary with skull size across strepsirrhines (Ross and Ravosa, 1993). Conventional data suggest that the anthropoid basicranial angle tends to ﬂex as skull size increases (Ross and Ravosa, 1993). When accounting for phylogenetic nonindependence, however, this correlation is no longer apparent (Table 1). When the two infraorders are considered independently, platyrrhines show a tendency toward size-related ﬂattening of the basicranium while catarrhines become more ﬂexed with size. When phylogeny is taken into account, the correlation between CBA and size is not signiﬁcant in platyrrhines. The degree of facial kyphosis shows little relationship with skull size across anthropoids or catarrhines (Table 1, Fig. 3c). Alternatively, platyrrhines show a trend (i.e., P \ 0.05) toward increasing facial kyphosis with skull size. Comparison among suborders and anthropoid infraorders Both conventional and IC ANCOVAs suggest that anthropoid JJH increases signiﬁcantly faster with skull size than strepsirrhines, although the IC result does not reach signiﬁcance after Bonferroni adjustment (Table 2, Fig. 3a) (Ravosa et al., 2000). It is apparent from Figure 3a that anthropoids (with the exception of callitrichids and squirrel monkeys) typically have on average taller jaw-joints than most strepsirrhines at a given skull size (Ravosa et al., 2000). Platyrrhines and catarrhines do not differ signiﬁcantly in JJH for the IC ANCOVA, but the conventional ANCOVA suggests that platyrrhine JJH increases more quickly with skull size (Table 2). Suborder comparisons for CBA demonstrate a signiﬁcant difference in y-intercept for the IC data with strepsirrhines having a less-ﬂexed cranial base (i.e., a larger CBA angle) than anthropoids for a given skull size American Journal of Physical Anthropology 524 B.A. ARMFIELD AND C.J. VINYARD Fig. 5. Plot of cranial base angle on facial kyphosis (symbols: l, Strepsirrhines; n, Platyrrhines; ~, Catarrhines). Fig. 4. Plot of relative ln jaw-joint height on (a) cranial base angle and (b) facial kyphosis (symbols: l, Strepsirrhines; n, Platyrrhines; ~, Catarrhines). (Table 2, Fig. 3b). Between anthropoid infraorders, the conventional data indicate that platyrrhine CBA increases at a signiﬁcantly faster rate than catarrhines. When examining IC data, this slope difference is not signiﬁcant; however, platyrrhines tend to have a signiﬁcantly less ﬂexed cranial base than catarrhines at a given skull size (Table 2, Fig. 3b). Anthropoids and strepsirrhines show no signiﬁcant differences in the AFK relative to skull size (Table 2, Fig. 3c). Similarly, platyrrhines and catarrhines show no statistical differences in AFK between infraorders in the conventional or IC ANOVA (Table 2). Correlations among relative JJH and cranial angles Prediction One suggests that increased basicranial ﬂexion will be correlated with relatively taller jaw joints in various primate clades. Strepsirrhines show no relationship between relative JJH and CBA (Table 3, Fig. 4a). Alternatively, anthropoids show a moderate semipartial correlation for the conventional and IC data (Table 3). These correlations, however, are positive indicating that relatively taller JJHs are associated with less ﬂexed cranial bases among anthropoids (Fig. 4a). This relationship runs contrary to Prediction One. American Journal of Physical Anthropology Further examination indicates that the observed association between CBA and relative JJH in anthropoids appears to be primarily related to the association of these two variables in platyrrhines (Fig. 4a). New World monkeys exhibit signiﬁcant positive correlations between CBA and relative JJH for both conventional and IC data (Table 3). Alternatively, catarrhines show no statistical relationship between these two variables. A broadly similar pattern is seen for correlations between AFK and relative JJH (Table 3, Fig. 4b). Prediction Two suggests that relative JJH increases with increasing ﬂexion in AFK. Strepsirrhines exhibit no association while anthropoids show some evidence for a positive association between AFK and relative JJH for the conventional data (P \ 0.05). Like Prediction One, this association is opposite to the predicted relationship between these variables. The association observed across anthropoids appears to be primarily due to the strong positive association of AFK and relative JJH among platyrrhines (Table 3). Catarrhines show no association between these variables. Finally, comparisons of AFK and CBA show no evidence of an association in strepsirrhines or catarrhines (Table 3, Fig. 5). Alternatively, anthropoids and platyrrhines exhibit a signiﬁcant correlation between these two angles for the conventional data. Ross and Ravosa (1993) observed similar clade-speciﬁc relationships (or lack thereof) between AFK and CBA. DISCUSSION We did not observe the hypothesized associations between relative JJH and either the basicranial angle (CBA) or AFK in the primate clades examined here. Furthermore, the three primate clades exhibited highly divergent relationships between relative JJH and these two angles. These observations raise questions about how clade-speciﬁc craniofacial growth inﬂuences their respective relationships between the posterior face and basicranium, how these patterns affect masticatory function across primates and how these clade-speciﬁc morphological patterns arose during primate evolution. 525 JJH ACROSS PRIMATES (Ross and Ravosa, 1993; Lieberman et al., 2000; Ross, 2000; McCarthy, 2001; Ross et al., 2004). First, JJH in primates appears to be inﬂuenced by multiple factors including those that impact CBA and facial angle (Ravosa et al., 2000; Bastir and Rosas, 2004; Lieberman et al., 2000, 2008). This mosaicism is clearly apparent in the interspeciﬁc data examined here, and we speculate that the interspeciﬁc pattern translates from the multifactorial set of inﬂuences that occur during growth within primates (Enlow, 1990; Jeffery, 2003, Bastir and Rosas, 2004; Lieberman et al., 2008). Second, these inﬂuences likely changed throughout the evolution of different primate lineages. This evolutionary divergence is most evident in the differences in JJH and CBA between primate suborders (Table 2; Figs. 3 and 6a). Finally, the mosaicism indicates that we are unlikely to identify a single satisfying structural explanation for the observed interspeciﬁc variation in JJH, or by extension posterior facial height, among primates. Future analyses may beneﬁt from considering phylogentically restricted groups of primates to highlight how changes in growth and integration patterns inﬂuence JJH in these restricted primate clades (e.g., Bastir and Rosas, 2004, 2005). Strepsirrhines Fig. 6. (a) Scatterplot of ln jaw-joint height on cranial base angle in primates. (b) Boxplot of ln jaw-joint height for strepsirrhines, platyrrhines, catarrhines, and speciﬁc fossil primates. Jaw-joint heights for fossil specimens were measured as described in the methods using scaled lateral-view photographs of the specimens published in the primary literature (symbols: l, Strepsirrhines; n, Platyrrhines; ~, Catarrhines). The mosaic pattern of JJH relationships in different primate clades We observed disparate patterns of correlations and scaling relationships for JJH relative to midline basicranial and facial angles among primate clades. Strepsirrhines differ from anthropoids in having on average lessﬂexed basicrania and absolutely shorter JJH (Fig. 6a). Within both strepsirrhines and catarrhines, however, relative JJH is unrelated to CBA and AFK. Platyrrhines show a third pattern where relatively taller JJH is correlated with less-ﬂexed basicrania and to a lesser extent more airorhynch faces. These differing relationships extend earlier observations that cranial base morphology exhibits a number of different relationships with facial form across primate clades and has several implications JJH in strepsirrhines shows at best a modest correlation with skull size and essentially no relationship with the midline CBA and facial angle (Tables 1 and 3). There are potentially several, nonmutually exclusive, explanations for this lack of association. In part, the small strepsirrhine samples for CBA and AFK likely contribute. More interestingly, the weak correlations across strepsirrhines may be partly due to differing relationships among strepsirrhine families. For example, cheirogaleids trend toward an absolute decrease in JJH with increasing skull size in contrast to most other strepsirrhine families. This tendency is largely due to the absolutely low-condyle position and large size of Phaner furcifer among cheirogaleids. In this instance, the pattern may be attributable to lowering of JJH in conjunction with increased gapes during tree gouging in this largest member of the clade (Vinyard et al., 2003). Galagonids show a less-striking, but similar pattern. The largest genus, Otolemur, also exhibits relatively low-condyle heights and feeds extensively on exudates (Williams et al., 2002; Burrows and Smith, 2005). Regardless of explanation, the observed lack of association among strepsirrhines recapitulates observations seen in previous studies examining CBA and facial morphologies (Ross and Ravosa, 1993). It is interesting to speculate that the lack of interspeciﬁc association may result from a lack of integration among these basicranial and facial components within strepsirrhine species. Because JJH has speciﬁc functional implications related to mastication, low levels of integration in strepsirrhines may indicate a relative ‘‘freedom’’ for independent evolution of JJH and posterior facial height when compared with many anthropoid species. Concomitantly, variation in strepsirrhine JJH may be more closely related to functional demands over integrated changes in cranial base-face architecture (Ravosa et al., 2000). Anthropoids: platyrrhines vs. catarrhines Anthropoid JJH scales with positive allometry relative to skull size (Table 1; Fig. 3a). Beyond this suborder American Journal of Physical Anthropology 526 B.A. ARMFIELD AND C.J. VINYARD scaling pattern, platyrrhines and catarrhines diverge markedly in their relationships between JJH and the two craniofacial angles. Platyrrhines exhibit moderate associations between relative JJH and both CBA and AFK, whereas catarrhines show no relationships (Table 3; Fig. 4). Thus, the signiﬁcant correlations among relative JJH, CBA, and AFK in anthropoids appear to result primarily from the relationships in New World monkeys (Table 3). The signiﬁcant associations in platyrrhines still fail to support our predictions as both the cranial base and face become less, rather than more, ﬂexed with relatively larger JJH. As typical of interspeciﬁc comparisons, the associations between relative JJH and both the basicranial and facial angles in platyrrhines may result from multiple underlying effects. These factors may impact all species in a clade or signiﬁcant interspeciﬁc associations can arise from speciﬁc evolutionary events affecting one or two clades within the larger group. Among platyrrhines, the derived craniofacial conﬁguration of howlers, potentially related to their enlarged hyoid apparatus and folivory (Beigert, 1963; Zingeser, 1973), and callitrichids, related to the reduced condylar height in the tree-gouging pygmy marmoset, extend the platyrrhine distribution (Figs. 4 and 5). Removing these extremes, however, does not alter the basic pattern observed across platyrrhines, suggesting that the group may share signiﬁcant associations among these craniofacial variables not found in other primate clades.4 The differences between platyrrhine and catarrhine skulls likely extend beyond the dimensions examined here as both CBA and AFK exhibit dissimilar relationships with skull size between the two clades (Ross and Ravosa, 1993) (Table 1; Fig. 3). For example, Bouvier (1986) identiﬁed several morphological differences in the masticatory apparatus of platyrrhines relative to catarrhines. Combining these results suggest that infraorder differences in craniofacial angles or masticatory apparatus form may be indicative of a larger pattern of disparity in craniofacial morphology between the two anthropoid infraorders. If true, then these differences in morphology imply that the two clades have experienced distinct evolutionary pressures on craniofacial form since their split from a common ancestor. Future work is needed to compare skull form in greater detail between these two infraorders. Finally, the different relationships among JJH, CBA, and AFK between platyrrhines and catarrhines raise an important consideration for interspeciﬁc studies across anthropoids. A key concern questions whether catarrhine and platyrrhine skulls differ sufﬁciently that combining them in a single group for analysis can mislead interpretations of skull form in the two infraorders. Although studies have demonstrated infraorder differences (e.g., Bouvier, 1986; Ross and Ravosa, 1993), conclusions based on combined analyses of catarrhine and platyrrhine species have also been common (e.g., Ravosa et al., 2000). On the basis of our results, we argue that additional analyses comparing platyrrhines and catarrhines might further our understanding of the evolutionary history of the anthropoid radiation. 4 We acknowledge that we cannot rule out the converse pattern that some catarrhines, such as the Old World monkeys (e.g., Delson and Rosenberger, 1984), possess a canalized craniofacial form underlying their lack of association among these variables. American Journal of Physical Anthropology The primate posterior face and its relationships with the midline versus lateral cranial base Recently, Bastir and colleagues have shown that the posterior face in humans and chimpanzees shares a stronger morphological association with the lateral compared to the midline basicranium (Bastir and Rosas, 2004, 2005, 2006; Bastir et al., 2004, 2006). Midline basicranial features are associated with the posterior face, however, these correlations tend to be weaker than those involving the lateral basicranium. As noted by Enlow (1990, p 209), the stronger association between the lateral basicranium and posterior face is not unexpected given that the actual contacts between growth counterparts involve lateral structures in the skull. Additionally, Bastir and Rosas (2006) hypothesize that the stronger association between the posterior face and lateral basicranium partly reﬂects their overlapping growth periods, providing greater opportunity for growth-related interactions, while the midline cranial base completes most of its growth earlier in ontogeny (Bastir and Rosas, 2006). Thus, our use of midline basicranial structures provides a convenient set of landmarks for comparative analysis, but may have a less direct relationship with the posterior face during growth. The observation that the posterior face may share more growth-related interactions with the lateral basicranium in hominoids has several implications for our results. First, while we demonstrate correlations between midline craniofacial angles and relative JJH, there may be stronger associations between relative JJH and the lateral basicranium. This hypothesis deserves further investigation to determine whether patterns observed in chimpanzee and human basicrania are found throughout primates. Second, differing patterns of integration between the midline and lateral basicranium may help explain the discordant results found between higher-order primate clades in this study as well as previous analyses of basicranial and facial form (Ross and Ravosa, 1993; Jeffery, 2003). As a hypothetical example, platyrrhines may exhibit higher levels of integration between midline and lateral basicranial structures, which may subsequently underlie the signiﬁcant associations between midline basicranial angulation and relative JJH in this clade. Third, the varying pattern of results across these major primate clades suggests that primates do not show a single pattern of integration between the basicranium and face. Extrapolating results from analyses of single species or single clades to primates as an order is a risky endeavor at best. Additional data from the basicranium, in particular, lateral structures, across a broader sample of primates are needed to address these issues. Functional implications for patterns of JJH variation Anthropoids on average have taller JJHs for a given skull size than strepsirrhines (Ravosa et al., 2000), whereas catarrhines exhibit a slight tendency to have relatively taller JJHs than platyrrhines (Table 2). Because JJH increases with positive allometry, these transpositions may be a consequence of the average larger size of anthropoids over strepsirrhines and catarrhines over platyrrhines (Fig. 3a). A relatively taller JJH has been argued to enhance masseter and medial pterygoid size and potentially moment arm lengths 527 JJH ACROSS PRIMATES (Greaves, 1974; Ward and Molnar, 1980; Freeman, 1988), more evenly distribute occlusal forces along the postcanine tooth row (Zingeser, 1973; Greaves, 1974; Ward and Molnar, 1980) and result in a more vertically-oriented masseter and medial pterygoid muscle resultant (Ravosa et al., 2000). Thus, size-correlated changes in relative JJH likely have speciﬁc functional consequences for masticatory behaviors across primates (Zingeser, 1973; Greaves, 1974, 1980, 1995; Herring and Herring, 1974; Osborn, 1987; McCollum, 1999; Ravosa et al., 2000; Sondang et al., 2003; Vinyard et al., 2003). The mosaic pattern of correlations and scaling relationships for JJH across different primate clades may indicate that the primate infraorders have experienced distinct functional demands related to feeding performance. Alternatively, variation in JJH may reﬂect correlated shifts in facial height resulting from evolutionary changes in CBA and facial angle throughout primate evolution (Ravosa et al., 2000). With the exception of platyrrhines, it does not appear that relative JJH is fundamentally linked to variation in basicranial and facial angulation across primates contrary to Ravosa et al. (2000). In the previous section, we argued that the potentially low levels of integration between JJH and craniofacial angulation in strepsirrhines may provide them a relative ‘‘freedom’’ for independent evolution of JJH compared to anthropoids. We can extend this argument to include catarrhines when compared with platyrrhines. In doing so, we generate a hypothesis predicting stepwise differences in the levels of integration between posterior facial height and craniofacial angulation across primates. Testing this hypothesis will help us to better understand the relative roles of size-related, developmental and dietary inﬂuences on posterior facial height in these different primate clades. Evolution of JJH in primates Anthropoids have diverged from strepsirrhines in several craniofacial features, including aspects of their masticatory apparatus and neurocranial dimensions linked to housing larger brains (Ross, 1996; Kay et al., 1997). The masticatory apparatus of anthropoids tends to exhibit more robust corpora (including fused symphyses), greater isognathy (i.e., the widths of upper and lower dental arcades are more similar), relatively large molar crushing surfaces, relatively isodontic molars (i.e., the upper and lower molars have more similar widths), and more vertically-oriented superﬁcial masseters compared to the average strepsirrhine (Hiiemae and Kay, 1973; Kay, 1975; Hylander, 1979; Ravosa, 1991, 1999; Ravosa and Hylander, 1994; Ravosa et al., 2000; Ross, 2000). The vertically-oriented superﬁcial masseters are linked to relatively tall mandibular rami and JJHs that also characterize anthropoids (Ravosa et al., 2000). Although the relatively taller JJH have speciﬁc functional consequences for mastication, it remains unclear whether changes in anthropoid facial heights reﬂect masticatory adaptations and/or correlated effects resulting from morphological shifts in other cranial regions. Anthropoids have on average both taller JJHs and more ﬂexed basicrania (CBA) than most strepsirrhines at a given skull size (Figs. 3 and 6a) (Ross and Ravosa, 1993; Ravosa et al., 2000). Suborder differences in both JJH and CBA support the hypothesis that changes in basicranial angulation in stem anthropoids may have signiﬁcantly inﬂuenced facial height and masticatory apparatus function in this clade (Ravosa et al., 2000). Additionally, JJH estimates in Parapithecus grangeri, an early anthropoid (Fleagle and Kay, 1987), and Rooneyia viejaensis, and an enigmatic Eocene fossil demonstrating anthropoidlike features (Szalay and Wilson, 1976; Rosenberger, 2006), are intermediate between strepsirrhines and anthropoids further supporting the plausibility of this evolutionary scenario (Fig. 6b). We lack the necessary data on CBA in early anthropoids to assess whether CBA and JJH are evolving simultaneously as further assessment of the hypothesis that cranial base ﬂexion initiated a cascade of developmental events resulting in the taller posterior facial heights observed in anthropoid primates (Ravosa et al., 2000).5 Our hypothesis tests demonstrate little support for the predicted relationship between increased relative JJH and cranial base ﬂexion in primates. In fact, platyrrhine primates show the strongest relationship between these dimensions, but increases in relative JJH are correlated with less-ﬂexed CBA throughout the clade. Our results suggest that if the observed differences in JJH between anthropoids and strepsirrhines are related to CBA, then this evolutionary event may have been limited to a relatively brief period at the origin of anthropoids. From a comparative perspective, we could hypothesize this distinct event as creating a ‘‘grade shift’’ in JJH between strepsirrhines and anthropoids. Failure to observe the predicted relationship between relative JJH and CBA across anthropoids suggests that these two features have been inﬂuenced by additional, and in many cases independent, factors during the evolution of the anthropoid infraorders. The stem catarrhine Aegyptopithecus zeuxis possesses an intermediate JJH that falls at the lower end of the catarrhine range of values (Fig. 6b) and may help establish the longevity of these distinct inﬂuences on the anthropoid infraorders. Although this speculation is interesting, additional work in fossil primates is needed to document the history of morphological changes in JJH and cranial angulation throughout anthropoid evolution. ACKNOWLEDGMENTS We thank the following institutions and individuals for providing access to primate skulls: Field Museum of Natural History (L. Heaney, B. Patterson, and W. Stanley); National Museum of Natural History (L. Gordon and R. Thorington); American Museum of Natural History (R. MacPhee); Natural History Museum, London (P. Jenkins); Muséum National d’Histoire Naturelle (J. Cuisin); Naturhistorisches Museum Basel (M. Sutermeister and F. Weidenmayer). B. Shea and D. Schmitt kindly allowed access to video capture and videometric analysis software. We thank two anonymous reviewers for numerous helpful comments that improved the manuscript. 5 Simons (2004) reports an estimated cranial base angle of 1578 for a single P. grangeri specimen (DPC 18651). Measurement details are not provided. Thus, we cannot directly compare this value to those used here. Simons (2004) does however indicate that this value for P. grangeri falls at the ﬂexed end of the strepsirrhine range (1578–1818) and within the anthropoid range (1358–1888) based on comparison with data from Ross and Ravosa (1993). American Journal of Physical Anthropology 528 B.A. ARMFIELD AND C.J. VINYARD APPENDIX A TABLE A1. Primate species and measurements included in the analysis Species Cheirogaleus major Cheirogaleus medius Microcebus murinus Microcebus rufus Mirza conquereli Phaner furcifer Avahi laniger Indri indri Propithecus diadema Propithecus verreauxi Eulemur coronatus Eulemur fulvus Eulemur macaco Eulemur mongoz Eulemur rubriventer Hapalemur griseus Hapalemur simus Lemur catta Varecia variegata Lepilemur dorsalis Lepilemur edwardsi Lepilemur leucopus Lepilemur microdon Lepilemur mustelinus Lepilemur ruﬁcaudatus Lepilemur septentrionalis Arctocebus aureus Arctocebus calabarensis Galago alleni Galago gallarum Galago matschiei Galago moholi Galago senegalensis Galagoides demidoff Galagoides zanzibaricus Otolemur crassicaudatus Otolemur garnetti Callimico goeldii Callithrix humeralifer Cebuella pygmaea Leontopithecus rosalia Saguinus fuscicollis Alouatta palliata Alouatta seniculus Aotus vociferans Ateles chamek Brachyteles arachnoides Callicebus cupreus Cacajao melanocephalus Cebus apella Chiropotes satanas Lagothrix lagotricha Pithecia pithecia Saimiri sciureus Allenopithecus nigroviridis Cercopithecus aethiops Cercocebus torquatus Cercopithecus mitis Erythrocebus patas Lophocebus albigena Macaca fascicularis Macaca nemestrina Mandrillus leucophaeus Miopithecus talapoin Papio anubis Theropithecus gelada Colobus guereza Nasalis concolor Family JJHa CBAb AFKb Cheirogaleidae Cheirogaleidae Cheirogaleidae Cheirogaleidae Cheirogaleidae Cheirogaleidae Indriidae Indriidae Indriidae Indriidae Lemuridae Lemuridae Lemuridae Lemuridae Lemuridae Lemuridae Lemuridae Lemuridae Lemuridae Megaladapidae Megaladapidae Megaladapidae Megaladapidae Megaladapidae Megaladapidae Megaladapidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Lorisidae Callitrichidae Callitrichidae Callitrichidae Callitrichidae Callitrichidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cebidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Cercopithecidae Colobinae Colobinae 2.41 1.18 2.67 2.10 2.61 0.813 5.57 10.14 9.78 8.04 3.99 4.22 5.37 4.60 5.17 3.35 8.64 5.45 4.25 4.66 5.17 4.14 4.28 4.26 4.25 4.50 4.37 3.47 4.18 2.85 2.77 3.85 3.04 2.99 3.70 3.52 2.07 6.96 3.29 1.29 6.74 2.52 28.15 32.65 6.70 11.78 21.80 7.04 9.37 9.49 9.72 13.90 7.56 2.42 13.61 10.14 20.03 11.82 8.59 17.86 15.69 18.03 27.22 7.57 22.15 39.90 16.76 10.24 186.8 154 142.8 189 138.2 183.7 186.2 153.2 166.3 184.8 137 183.7 158 179.5 144.2 187.8 181.2 143.2 194.4 156.7 178.7 155.8 165 141.5 164.2 172.5 164.5 180.7 141.5 154.5 140 174.8 172.5 159.4 166.6 169.5 176 175.8 165.5 154.2 169.9 151.4 162 135.3 157.3 170 158.7 161.5 142 142.8 134.8 163.8 155 164.2 153.2 156.5 130.6 150 175.3 146.8 160.2 160.8 SkullGMc 21.74 16.17 11.87 12.20 19.46 20.23 21.68 40.76 36.26 33.25 31.40 35.40 36.06 32.06 35.76 26.75 36.40 31.72 42.33 22.13 22.58 19.95 22.85 23.63 22.60 21.59 18.25 21.25 19.35 16.61 15.88 15.40 16.62 13.24 16.08 27.57 26.21 . 18.73 13.38 22.79 18.79 44.42 46.57 23.68 41.53 46.58 24.70 34.34 38.80 31.99 40.03 29.71 22.28 38.82 39.46 51.66 40.29 48.51 46.06 45.93 52.66 71.01 26.38 72.15 67.42 45.91 39.74 (continued) American Journal of Physical Anthropology 529 JJH ACROSS PRIMATES TABLE A1. (Continued) Family JJHa Colobinae Colobinae Colobinae Colobinae Colobinae Colobinae Colobinae Hylobatidae Hylobatidae Hominidae Hominidae Hominidae 13.94 8.67 11.97 10.08 14.55 15.78 11.32 12.41 18.44 65.50 32.73 64.22 Species Nasalis larvatus Presbytis rubicunda Procolobus rufomitratus Procolobus verus Pygathrix nemaeus Rhinopithecus roxellana Trachypithecus obscura Hylobates lar Hylobates syndactylus Gorilla gorilla Pan troglodytes Pongo pygmaeus CBAb AFKb SkullGMc 159 166.5 171.4 156.1 157.2 161.3 143.8 161 154.5 143.5 143.8 168.3 158.3 157.3 158.7 160.8 150.2 123 138.8 46.96 36.51 41.78 34.67 43.13 47.20 39.85 39.98 48.67 100.13 75.30 91.54 a Jaw-joint height (JJH) taken from Vinyard (1999). Values are in mm. Cranial base angle (CBA) and the angle of facial kyphosis (AFK) were taken from Lieberman et al. (2000). Values are in degrees. c The skull geometric mean (SkullGM) is based on the following linear dimensions taken from Vinyard (1999): (1) mandible length, (2) palate length, (3) nasion–prosthion height, (4) cranial length, (5) bizygomatic breadth, (6) biglenoid breadth, (7) M1 width, (8) basion–nasion length, (9) palate breadth at M1, and (10) mandibular arch breadth at M1. Values are in mm. b APPENDIX B Composite phylogeny used in phylogenetic comparative analyses. Phylogenies were adapted from Purvis (1995), Smith and Cheverud (2002) and Vinyard and Hanna (2005). Phylogeny in Nexus format. ((((((G.matschiei,(G.alleni,(G.zanzibaricus,G.demidoff))), (G.moholi,(G.gallarum,G.senegalensis))),(O.garnetti, O.crassicaudatus)),(A.aureus,A.calabarensis)),((((L. septentrionalis, (L.ruﬁcaudatus,(L.leucopus,(L.edwardsi, L.dorsalis)))),(L.mustelinus,L.microdon)),((V.variegata, ((L.catta,(H.griseus,H.simus)),(E.rubriventer,((E.fulvus, E.mongoz),(E.macaco,E.coronatus))))),(A.laniger,(I.indri, (P.diadema,P.verreauxi))))),(P.furcifer,((M.conquereli, (M.murinus,M.rufus)),(C.major,C.medius))))),(((A.vociferans, (((C.pygmaea,C.humeralifera),(L.rosalia,S.fuscicollis)), (C.apella,S.sciureus))),((C.albicans,(C.satanas,(C.melanocephalus,P.pithecia))),((B.arachnoides,(A.chamek,L. lagotricha)),(A.palliata,A.seniculus)))),((((A.nigroviridis, (C.mitis,(M.talapoin,(C.aethiops,E.patas)))),((M.fascicularis, M.nemestrina),((M.leucophaeus,C.torquatus),(L.albigena, (T.gelada,P.anubis))))),((C.guereza,(P.versus,P.rufomitratus,)), (((P.rubicunda,,T.obscurus),(N.larvatus,N.concolor)),(P.nemaeus, R.roxellana)))),((H.lar,H.syndactylus),(P.pygmaeus,(G.gorilla, P.troglodytes)))))) LITERATURE CITED Bastir M, Rosas A. 2004. 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