The mental foramen marks the location where the inferior alveolar nerve and blood vessels exit the mandibular canal to become the mental nerve and blood vessels. Its position with respect to the tooth row has been recorded by researchers as a distinctive taxonomic character for over a 100 years (Williams and Krovitz, 2004). However, nonmetric taxonomic analyses of the antero/posterior (A/P) position of mental foramen relative to specific dental elements have been plagued by differences in the timing of dental eruption events among species and also variation in tooth size among males and females, both within and between species. Establishing a method to quantify the A/P position of the mental foramen should enable researchers to make more accurate comparisons within and across primate taxa.
Efforts to quantitatively assess the position of the mental foramen in fossil hominins have focused on late Pleistocene Homo specimens (Rosas, 1997, 2001; Williams and Krovitz, 2004). Quantitative studies of this character on extant hominoids and earlier fossil hominin taxa have not been published.
MENTAL FORAMEN POSITION AS A NONMETRIC TRAIT IN EXTANT HOMINOIDS
Nonmetric observations of mental foramen A/P position relative to the dentition have often been featured as taxonomic characters separating extant hominoid and fossil hominin lineages (Groves, 1970, 1986; Condemi, 1991; Hublin, 1998; Coqueugniot, 2000). However, some researchers have disputed the utility of this qualitative character to differentiate hominoid taxa given the extent of its intraspecific variability (Wood and Chamberlain, 1986; Brown, 1989) and because the mental foramen and the dentition have distinct embryological origins (Trinkaus, 1993).
Most studies have described the modal position of the mental foramen along the dental arcade as the same (inferior to P4) in all great ape species and modern human populations (Simonton, 1923; Schulz, 1933; Tebo and Telford, 1950; Wood and Chamberlain, 1986; Brown, 1989; Trinkaus, 1993). Other researchers have argued that there are significant differences in this character among extant hominoid species. For example, Aitchison (1965) described the mental foramen as inferior to the distal aspect of P3 in Pan troglodytes and Gorilla gorilla, but characterized it as inferior to P4 in Pongo pygmaeus. Other studies have reported that the mental foramen is positioned posterior to P4 more frequently in P. troglodytes than in G. gorilla and P. pygmaeus (Simonton, 1923; Montagu, 1954). Robinson (2003) found that when mandibles are scaled to unit centroid size the mental foramen is more anteriorly placed on gorilla mandibles than on those of other extant hominoids.
The A/P position of the mental foramen has also been cited as a means of differentiating Gorilla subspecies (Vogel, 1961; Groves, 1970, 1986; Goodall and Groves, 1977; Groves and Stott, 1979; Robinson, 2003). Researchers have described the mental foramen as most commonly positioned under P4 or P3 in G. g. gorilla, P3 in G. g. graueri, and P3 or C in G. g. beringei (Vogel, 1961; Groves, 1970, 1986). Using geometric morphometric techniques, no significant differences were found in the mean A/P position of the mental foramen among Pan troglodytes or Pongo pygmaeus subspecies when individuals were scaled to unit centroid size (Robinson, 2003).
Quantifying the A/P position of the mental foramen would enable researchers to more accurately assess whether there are significant differences among extant hominoid taxa for this character. If significant interspecific diversity is found among hominoids, this would suggest that the A/P position of the mental foramen is worth investigating as a character that may be important in differentiating fossil hominoid species. However, if the extent of intraspecific variation among extant hominoids is so great that it is not possible to significantly differentiate any extant hominoid species from any other, this could be seen as evidence that the A/P position of the mental foramen is not taxonomically informative in hominoids and that any differences among putative fossil taxa could represent normal intraspecific variation.
MENTAL FORAMEN POSITION IN AUSTRALOPITHECUS
Australopithecus africanus and A. afarensis have been described as exhibiting the same modal A/P position of the mental foramen (i.e., inferior to P4, with its position varying from P3 to P4/M1 in both species) (Tobias, 1991; Robinson, 2003). The three Australopithecus anamensis mandibles retaining the mental foramen encompass this entire range. The mental foramen is located inferior to the distal segment of P3 in KNM-KP 29287 and below P4/M1 in the type specimen, KNM-KP 29281 (Ward et al., 2001). Robinson (2003) found no significant differences among the three Australopithecus species in the mean A/P position of the mental foramen when specimens were scaled to unit centroid size.
Most scholars today regard the mandibular specimens from Hadar, Maka, and Laetoli to be part of a single species, Australopithecus afarensis, that is taxonomically distinct from the Australopithecus africanus specimens from Taung, Sterkfontein, and Makapansgat in South Africa (e.g., Johanson and White, 1979; White et al. 1981; Wood, 1991; Wood and Richmond, 2000). However, some dispute the taxonomic unity of the specimens attributed to the two species (e.g., Olson, 1981, 1985; Senut and Tardieu, 1985; Clarke, 1988; Senut, 1996), whereas others have argued that A. afarensis and A. africanus represent a single taxon (Tobias, 1980; Logan et al. 1983; Schmid, 1983). As a preliminary investigation into fossil hominin diversity for the A/P position of the mental foramen, we explore differences in this feature among available mandibles attributed to Australopithecus africanus and A. afarensis.
STRUCTURAL CONSTRAINTS ON MENTAL FORAMEN POSITION
As is clear from a cursory examination of mandibular form, modern humans have absolutely shorter jaws than extant hominoids. Significant differences have also been found between great apes in the absolute and relative lengths of their dental arcades (Weidenreich, 1936; Goodman, 1968; Hylander, 1988; Jenkins, 1990; Humphrey et al., 1999; Taylor, 2002; Taylor and Groves, 2003). It may be that changes in the length of the mandible within and/or among taxa affect where the inferior alveolar nerve and blood vessels exit the mandibular corpus. For example, there may be a structural constraint on the absolute length of the mandibular canal such that larger individuals have more posteriorly positioned mental foramina. Alternatively, the anterior or posterior dentition may contribute disproportionately to elongating the dental arcade, leading to more posteriorly or anteriorly positioned mental foramina, respectively. Thus, it is important to explore how the A/P position of the mental foramen changes in concert with an increase in dental arcade length.
Another significant difference between hominins and the great apes is the overall size of their canines, and the degree of canine dimorphism. Enlarged canine roots may influence where the inferior alveolar nerve and blood vessels exit the mandibular corpus by limiting the anterior extension of the mandibular canal, resulting in a relatively more posteriorly positioned mental foramen. Consequently, the A/P position of the mental foramen may correlate with canine size among hominoid taxa and those species with stronger canine dimorphism may exhibit increased intraspecific variation in this character. Moreover, Australopithecus and Homo may show a more stable modal A/P position compared with other hominoids (i.e., reduced intraspecific variation).
Extant hominoids also differ in the extent to which the left and right mandibular corpora converge anteriorly. Generally, modern humans have been described as having anteriorly converging dental arcades, because of reduction in the size of their anterior dentition, whereas the tooth rows of extant great apes are portrayed as parallel-sided (e.g., Weidenreich, 1936; Straus, 1949; DuBrul and Sicher, 1954; LeGros Clark, 1964; Simons, 1972; Wood and Chamberlain, 1986; Daegling, 1993; Begun, 1994). Some researchers have also described differences in the extent to which the tooth rows converge anteriorly in great apes (Weidenreich, 1936; Andrews, 1978). Wood and Chamberlain (1986), however, found significant range overlap and nearly identical mean values in Gorilla gorilla, Pan troglodytes, and Pongo pygmaeus for the ratio of intercanine breadth to inter-M2 breadth. Variation in the degree of anterior convergence may influence the length of the mandibular canal, with a concomitant change in mental foramen A/P position.
NULL HYPOTHESES TO BE TESTED
No one has yet quantitatively analyzed the A/P position of the mental foramen across hominoids. Here, we assess the position of the mental foramen in the mandibles of extant great apes, humans and Australopithecus to test the following null hypotheses:
1There are no significant differences among extant hominoid taxa for mental foramen A/P position;
2There are no significant differences between the sexes of each species for this trait;
3Dental arcade length, canine size, and the extent of anterior convergence do not significantly influence intraspecific or taxonomic variation in mental foramen A/P position.
MATERIALS AND METHODS
The extant sample in this study consisted of 415 adult mandibles of humans (Homo sapiens), bonobos (Pan paniscus), chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongo pygmaeus) (Table 1). Data were gathered on individuals of each traditionally recognized subspecies of Gorilla gorilla (i.e., G. g. beringei, G. g. gorilla, and G. g. graueri), Pan troglodytes (i.e., P. t. schweinfurthii, P. t. troglodytes, and P. t. verus), and Pongo pygmaeus (i.e., P. p. abelii and P. p. pygmaeus). Homo sapiens specimens from four geographically distinct groups, eastern Asians, eastern Europeans, Melanesians, and western Africans, were included to incorporate a broad range of modern human variation. Data were collected at 11 museums in the United States and Europe (see Table 1). As efforts were made to obtain data on as many individuals as possible, taxonomic groups do not include equal numbers of males and females. Nonhuman hominoids were allocated to sex based on data from museum records and by examining canine size and shape. Modern human skulls were sexed using museum records and standard osteological criteria (Buikstra and Ubelaker, 1994). Data were collected on only wild shot extant hominoid specimens with M3 fully erupted; these specimens exhibited no obvious abnormalities and no substantial resorption because of antemortem tooth loss.
AMNH = American Museum of Natural History, New York; ASM = Anthropologische Staatssammlung, Munich; BMNH = British Museum of Natural History, London; MCZ = Museum of Comparative Zoology, Harvard; MRAC = Musée Royal de L'Afrique Centrale, Tervuren, Belgium; NMNH = National Museum of Natural History (Smithsonian); NNM = Nationaal Natuurhistorisch Museum, Leiden; PCM = Powell-Cotton Museum, Birchington, UK; PM = Peabody Museum, Harvard; ZMB = Zoologische Museum, Berlin; ZSM = Zoologische Staatssammlung, Munich.
Gorilla gorilla beringei
Gorilla gorilla gorilla
50 (27M, 23F)
AMNH, NNM, PCM, ZMB
Gorilla gorilla graueri
31 (19M, 12F)
AMNH, BMNH, MCZ, MRAC, NMNH, ZMB
Homo sapiens – Eastern Asia
21 (8M, 13F)
Homo sapiens – Eastern Europe
46 (23M, 23F)
Homo sapiens – Melanesia
25 (12M, 13F)
Homo sapiens – Western Africa
25 (16M, 9F)
25 (7M, 18F)
AMNH, BMNH, MCZ, MRAC
Pan troglodytes schweinfurthii
27 (19M, 8F)
AMNH, BMNH, MRAC, NMNH, PCM
Pan troglodytes troglodytes
46 (24M, 22F)
AMNH, MCZ, NNM, PCM, ZMB
Pan troglodytes verus
30 (15M, 15F)
AMNH, BMNH, NMNH, NNM, PM
Pongo pygmaeus abelii
38 (19M, 19F)
ASM, MCZ, NMNH, NNM, ZMB, ZSM
Pongo pygmaeus pygmaeus
35 (16M, 19F)
AMNH, ASM, BMNH, MCZ, NNM, NMNH
The fossil sample was comprised of five mandibular specimens attributed to Australopithecus afarensis housed at the National Museum of Ethiopia in Addis Ababa and one Australopithecus africanus mandible housed at the Department of Anatomical Sciences, University of the Witwatersrand, Johannesburg, South Africa (Table 2). These Australopithecus specimens were included because they were the only available mandibles that preserved the osteological landmarks necessary to quantify mental foramen A/P position.
NME = National Museum of Ethiopia; WITS = University of the Witwatersrand Medical School.
AL 288-1, AL 417-1, AL 437-1, AL 444-2b
Makapansgat, South Africa
Data were gathered using the MicroScribe-3DX, a digitizer that captures the three dimensional coordinates of landmarks. To calculate mental foramen A/P position, four type I and type II landmarks were digitized on each mandible (Fig. 1a) (Bookstein, 1990; Valeri et al. 1998). To determine the extent of dental arcade anterior convergence, abbreviated within this article as “anterior convergence,” four additional type II landmarks were digitized (Fig. 1b). Type I landmarks are contact points between structures, such as the intersection of two sutures, or the midpoints of foramina, whereas type II landmarks are points at the maxima of curvature, such as points on the maxima of tori and the minima of sulci (Bookstein, 1990; MacLeod, 2001). All fossil mandibles other than the nearly complete mandibular specimen from Maka, Ethiopia (MAK-VP 1/12), had either the left or right posterior M3 point missing. To increase the number of fossil specimens in our study, mirror imaging in GRF-nD (generalized rotational fitting of n-dimensional landmark data; Slice, 1994) was used to reconstruct the position of the missing posterior M3 landmark, using the more complete side.
Landmark data were converted to linear distances for analysis. Using the four mental foramen A/P position landmarks, two linear distances were calculated for all specimens, dental arcade length and the distance between the A/P position of the mental foramen on the midline dental arcade chord, abbreviated below as midline chord, and infradentale (mental foramen A/P distance). The first variable, dental arcade length, was measured as the distance between infradentale and the midpoint between the left and right posterior M3 points (M3 midpoint) (line A, Fig. 1a). The second variable, mental foramen A/P distance, was obtained by calculating (1) the distance between the mental foramen and infradentale (line B, Fig. 1a); (2) the distance between the midline chord (line A) and the mental foramen (line C, Fig. 1a) using the formula for the shortest distance between a point and a line and; (3) using the Pythagorean theorem, the distance between infradentale and the A/P position of the mental foramen on the midline chord (line D = mental foramen A/P distance, see Fig. 1a). It is important to note that using this method, the infero/superior position of the mental foramen and the breadth of the mandibular corpus do not affect the length of line D (i.e., mental foramen A/P distance), and thus, do not influence the results presented below.
We chose to determine the A/P position of the mental foramen along the midline chord primarily because the literature on this variable focuses on the location of the mental foramen relative to the dentition (e.g., Simonton, 1923; Groves, 1970, 1986; Condemi, 1991; Trinkaus, 1993; Franciscus and Trinkaus, 1995; Hublin, 1998; Quam and Smith, 1998; Coqueugniot, 2000; Lebel et al. 2001; Rosas, 2001). By quantifying the A/P position of the mental foramen in this manner, our results can be more easily compared with those of previous researchers. This dataset is not directly comparable with qualitative analyses because the position of the mental foramen relative to the individual dental elements is affected by dimorphism in the canine and the honing premolar (P3) and the relative lengths of the anterior and posterior dentition. Because of these factors, the A/P position of the mental foramen along the midline chord can be different from the position of the mental foramen with respect to the individual dental elements, and two individuals can differ in the former but exhibit the same value for the latter, and vice versa.
In exploring how the length of the mandible influences mental foramen A/P position, we chose to use dental arcade length rather than, for example, mandibular length (e.g., gnathion to gonion) because of a number of factors related to sexual dimorphism that could potentially influence measures of the overall length of the mandible. For example, the heavy insertions of the masseter and medial pterygoid muscles on the ascending ramus of large males (Daegling, 1996) probably contribute substantially to differences in mandibular length between males and females among sexually dimorphic hominoids. This may explain why in African apes, particularly among Gorilla subspecies, males have wider rami than females (Taylor and Groves, 2003). Thus, our measure of “mandibular size” (i.e., dental arcade length) captures the length of the tooth row in a standardized manner, without the possible confounding factor of ascending ramus width. Moreover, the ramus is rarely preserved in early hominin fossils and for nearly all Australopithecus mandibles it is not possible to measure gnathion to gonion.
The position of mental foramen (mental foramen A/P position) was calculated for all specimens by dividing mental foramen A/P distance by dental arcade length. We subjected the resulting data to a one-sample Kolmogorov–Smirnov analysis to test for significant departures from a parametric distribution. As the data were not normally distributed (P < 0.0001), nonparametric Kruskal–Wallis ANOVA analyses were run to evaluate whether the mean values of mental foramen A/P position were significantly different across extant and fossil hominoid subspecies and species. These tests were conducted for extant hominoid males and females separately, and then all specimens in each species together for comparisons with the fossil specimens for which sex is not known.
To explore how dental arcade length influences mental foramen A/P position and to compare the scaling of this variable among hominoid species, the log of mental foramen A/P distance was plotted against the log of dental arcade length for males and females of each species. Least-squares (LS) regression equations and correlation coefficients (r) were calculated for males and females of all extant subspecies and species. For comparisons with Australopithecus, these data were also calculated with males and females pooled.
A benefit to using log-transformed data is the ease with which allometry can be identified, such that if the confidence interval around an estimated slope overlaps 1.0, the null hypothesis of isometry cannot be rejected. Slope values significantly greater than 1.0 are positive, whereas those significantly less than 1.0 can be described as negatively allometric. For each taxon, with the sexes separated and then pooled for comparisons with Australopithecus, confidence intervals were calculated by adding and subtracting the standard error of the slope multiplied by the corresponding t value obtained from the t-distribution, which is based on the degrees of freedom.
To determine whether there were significant differences between the taxa in how mental foramen A/P distance scaled relative to “size” (i.e., dental arcade length), an ANCOVA was used, which tested for the homogeneity of slopes and their associated y-intercepts. Significance was inferred by comparing the slope values to the estimated confidence intervals for each taxon with the sexes both separated and then pooled. If the slopes were not significantly different, then the y-intercepts were tested for significance using the same procedure as for the slope values to determine whether two taxa shared a similar scaling pattern but one taxon was displaced above another indicating a more posteriorly positioned mental foramen at any size.
ANCOVA was developed using log-transformed data with LS regression (Sokal and Rohlf, 1995). Although reduced major axis (RMA) and other Model II methods have been applied to ANCOVA (e.g., Leigh et al., 2003), slope values under RMA are equivalent to LS slope values divided by the correlation coefficient. As log-transformation already decreases the correlation coefficient, using RMA would unnecessarily increase confidence limits.
To further explore potential influences on intraspecific and interspecific variation in mental foramen A/P position, a principal components analysis was run using mental foramen A/P distance, dental arcade length, anterior convergence of the tooth rows, and canine crown size (the product of the mesio-distal and bucco-lingual dimensions of the mandibular canines taken at the dento-enamel junction), each divided by the geometric mean to standardize for size differences. This multivariate analysis of the variables shows the relative contributions of traits to the placement of individuals along the axes. A multiple linear regression was also conducted to show the relative strength of dental arcade length, anterior convergence, and canine crown size in explaining variation in mental foramen A/P distance.
Intraspecific Analyses of Mental Foramen A/P Position
Pan troglodytes subspecies.
For mental foramen A/P position, no significant differences were found among males or females of the Pan troglodytes subspecies (Table 3).
Table 3. Mental foramen A/P position for great ape subspecies
Gorilla gorilla beringei
Gorilla gorilla gorilla
Gorilla gorilla graueri
Pan troglodytes schweinfurthii
Pan troglodytes troglodytes
Pan troglodytes verus
Pongo pygmaeus abelii
Pongo pygmaeus pygmaeus
Pongo pygmaeus subspecies.
No significant differences were found between females of the two Pongo pygmaeus subspecies for mental foramen A/P position (Table 3). Male P. p. abelii specimens had significantly more anteriorly positioned mental foramina than male P. p. pygmaeus specimens (P < 0.05), although considerable range overlap was found between these two taxa.
Gorilla gorilla subspecies.
There were no significant differences between male or female Gorilla gorilla graueri and G. g. beringei for mental foramen A/P position (Table 3). G. g. gorilla was significantly distinct from the other two subspecies for this variable using both the male and female datasets (P < 0.001) and its ranges only slightly overlapped those of the other two subspecies. When log mental foramen A/P distance was plotted against log dental arcade length, the G. g. gorilla specimens were positioned well above the eastern gorilla subspecies at similar dental arcade lengths, with little overlap in range (Fig. 2). This indicates that the mental foramen is more posteriorly positioned in western lowland gorillas. As G. g. gorilla was significantly different from the eastern subspecies in both the male and female datasets, it was examined separately in the analyses of species differences below.
Interspecific Comparisons of Male Extant Hominoids
Males of the two eastern Gorilla gorilla subspecies and Homo sapiens were significantly different from males of all other groups, other than eastern Gorilla males from Pan paniscus males, in exhibiting more anteriorly positioned mental foramina (Table 4). Pan troglodytes males had significantly more posteriorly placed mental foramina than males of all species other than Pongo pygmaeus. For males, there were no significant differences among Gorilla gorilla gorilla, Pan paniscus, and Pongo pygmaeus for mental foramen A/P position.
Table 4. Interspecific comparisons of mental foramen A/P position
Eastern Gorilla gorilla
Gorilla gorilla gorilla
Interspecific Comparisons of Female Extant Hominoids
In females, Homo sapiens and the two eastern Gorilla gorilla subspecies were found to have significantly more anteriorly positioned mental foramina than females of all taxa other than western G. gorilla (Table 4). Unlike in males, female Gorilla gorilla gorilla specimens had significantly more anteriorly positioned mental foramina than Pan paniscus females. This difference between the results for male and female western gorillas is not unexpected given that this variable was strongly sexually dimorphic in gorillas, with females having more anteriorly positioned mental foramina than males (see below). Pan troglodytes females had significantly more posteriorly placed mental foramina than females of all species other than Pan paniscus. Female Pan paniscus and Pongo pygmaeus could not be significantly differentiated from one another.
Interspecific Comparisons of Extant Hominoids with Australopithecus
When males and females were pooled for comparisons with the Australopithecus specimens, the significance tests on mental foramen A/P position split extant hominoid species into three groups: (1) the two eastern Gorilla gorilla subspecies and Homo sapiens, which had the most anteriorly positioned mental foramina, (2) Gorilla gorilla gorilla, Pan paniscus, and Pongo pygmaeus and, (3) Pan troglodytes, which had the most posteriorly placed foramina (Table 4). All of the taxa in these groups were significantly different from all taxa in the other two groups (P < 0.0001) other than the two Pan species, which could not be significantly differentiated. A. afarensis was significantly separated from all extant taxa other than those in group 1 (i.e., those possessing the most anteriorly positioned mental foramina) and western gorillas. The A. africanus specimen from Makapansgat (MLD 18) exhibited a more posteriorly placed mental foramen than all of the A. afarensis specimens (Table 4).
When log mental foramen A/P distance was plotted relative to log dental arcade length most of the fossils attributed to Australopithecus fell outside the ranges for extant taxa (Fig. 3). The location of MLD 18 on the bivariate plot was closest to the LS regression line estimated for modern humans (Fig. 3). In spite of having dental arcades that were similar in length to those of Pan and MLD 18, the five A. afarensis specimens had a shorter distance between infradentale and mental foramen, an indication of their more anteriorly positioned mental foramina. The larger A. afarensis specimens overlapped the range of female Pongo pygmaeus.
Size and Scaling
Mental foramen A/P distance scaled in a consistent manner with respect to dental arcade length in all extant hominoid taxa (P < 0.001 for all groups). In Australopithecus afarensis and all extant hominoid taxa (pooled datasets), other than Pan troglodytes, the regression slopes for mental foramen A/P distance compared to dental arcade length were greater than 1.0 (i.e., the mental foramen was positioned relatively more posteriorly along the midline chord in specimens with longer dental arcades) (Table 5). However, the regression slopes for Pan troglodytes, eastern Gorilla gorilla, and Australopithecus afarensis did not differ significantly from isometry. Most of the taxa which exhibit pronounced sexual dimorphism, namely Pongo pygmaeus and Gorilla gorilla gorilla, are positively allometric suggesting that males, with respect to females, have more anteriorly positioned mental foramina than expected. The eastern subspecies of Gorilla would most likely exhibit significant positive allometry if the variation in mental foramen A/P distance was not so extreme in females. For eastern gorilla males, the lower end of the confidence interval barely overlaps isometry (0.994). When the sexes are separated, the null hypothesis of isometry could only be confidently rejected for male and female Homo sapiens suggesting that in great ape taxa the difference between males and females is driving the positive allometry observed.
Table 5. ANCOVA results
Species with sexes pooled
Upper CI y-int.
Lower CI y-int.
Upper CI slope
Lower CI slope
Significantly different from isometry?
Eastern G. gorilla
Western G. gorilla
Upper CI y-int.
Lower CI y-int.
Upper CI slope
Lower CI slope
Significantly different from isometry?
Eastern G. gorilla
Western G. gorilla
Upper CI y-int.
Lower CI y-int.
Upper CI slope
Lower CI slope
Significantly different from isometry?
Eastern G. gorilla
Western G. gorilla
In the ANCOVA with the sexes pooled, the slope value for Australopithecus afarensis is most similar to that of Pongo but is only significantly different from that of Pan troglodytes (Table 5). With respect to its y-intercept value, it is significantly distinct only from eastern Gorilla gorilla. Pan troglodytes exhibited a significantly lower slope value compared with all other taxa. Homo sapiens and the eastern Gorilla subspecies exhibited the highest slope values and differed significantly from Pan troglodytes and Pongo pygmaeus (Table 5). Although eastern gorillas and modern humans exhibited similar slope values, their y-intercepts differed significantly. Pongo pygmaeus exhibited nonsignificant differences in slope and y-intercept values with all taxa except Pan troglodytes.
The ANCOVA comparison of slopes for males showed eastern gorillas, humans and bonobos all having significantly greater values than those of orangutans and chimpanzees. Western Gorilla males were significantly distinct in slope only from Pan troglodytes males and their y-intercept value differed significantly only from that estimated for Homo sapiens (Table 5). It is not surprising that the slope and y-intercept values associated with western Gorilla gorilla males yielded nonsignificant differences with Pongo pygmaeus males given the large confidence interval for Pongo.
Female eastern Gorilla gorilla, Homo sapiens, and Pan paniscus had significantly greater slopes than those of Pongo pygmaeus, Pan troglodytes, and Gorilla gorilla gorilla. Eastern gorilla females had a significantly greater slope than H. sapiens and had a significantly different y-intercept value than that of P. paniscus. Pan paniscus and H. sapiens were not significantly different for slope or y-intercept values. Pongo pygmaeus and Pan troglodytes females both exhibited relatively low slopes that were not significantly different but the two differed significantly in their y-intercept values. Western Gorilla females exhibited significantly lower slope values than those attributed to Homo sapiens and Pan paniscus.
Patterns of Sexual Dimorphism
Mental foramen A/P position exhibited no significant sexual dimorphism in any of the Pan troglodytes subspecies or P. paniscus (Tables 3 and 4). There was also no appreciable dimorphism in Homo sapiens for this variable (Table 4). Male and female orangutans of both subspecies were significantly different from one another (P < 0.05), with males exhibiting more posteriorly positioned mental foramina (Table 3). There was also a significant difference between males and females in all gorilla subspecies with males having more posteriorly positioned mental foramina (P < 0.05), although the difference was much greater in Gorilla gorilla beringei, with the ranges of the sexes nonoverlapping (Table 3).
Males and females tend to have similar slope and y-intercept values in every case except for Gorilla gorilla gorilla. This is particularly true in Pan paniscus and Pongo pygmaeus where the slope estimates for males and females are quite similar (Table 5). Another general trend is that the slope estimates for females within each species tend to be slightly more elevated than those for males. In those taxa for which males and females had similar y-intercept values this difference between the sexes reflects the more anteriorly positioned mental foramina of females compared with their male counterparts.
To investigate whether this pattern of dimorphism holds for A. afarensis, which is thought to be at least moderately dimorphic in body size (e.g., McHenry, 1991, 1992, 1994a; Richmond and Jungers, 1995; Lockwood et al. 1996; Plavcan and van Schaik, 1997a; cf. Reno et al. 2003) but exhibits reduced dimorphism in canine size (Johanson and White, 1979; Lovejoy, 1981; Leutenegger and Shell, 1987; McHenry, 1992, 1994a, b; Plavcan and van Schaik, 1994, 1997a), the specimens were divided into presumed male (i.e., A.L. 438-1 and A.L. 444-2) and presumed female (i.e., the Maka mandible, A.L. 288-1 and A.L. 417-1) groups (Johanson et al. 1982; Kimbel et al. 1994, 2004; White et al. 2000). The putative A. afarensis males and females had nonoverlapping ranges, although the difference between their means was slight (male mean = 0.27; female mean = 0.24), similar to the degree of dimorphism reported above for Pan and Homo sapiens.
To further explore how variables related to sexual dimorphism and dental arcade size and shape influence the A/P placement of the mental foramen, a multiple linear regression was performed comparing canine area, dental arcade length, and anterior convergence, to mental foramen A/P distance, each scaled to the geometric mean. All of the covariates showed a significant relationship with mental foramen A/P distance for males and females across taxa, except in the limited sample of Pan paniscus males in which only anterior convergence was significantly associated with mental foramen A/P distance (P < 0.001). The coefficients associated with the prediction of mental foramen A/P distance were all negative, with the largest values consistently associated with anterior convergence scaled to the geometric mean. Coefficients associated with relative anterior convergence were often one or two orders of magnitude greater than those associated with canine area and dental arcade length suggesting that anterior convergence scaled with respect to size strongly influences variation in mental foramen A/P distance.
A principal components analysis of the data scaled to the geometric mean produced two eigenvalues over 1.0 (2.338 and 1.006, respectively), and together those PC axes explained 83.6% of the variance (58.5 and 25.1%, respectively). The first PC axis appeared to be primarily driven by canine size, polarizing those individuals with proportionally large canines from those with proportionately smaller canines (Fig. 4). Modern humans lay on the positive end of this axis and barely overlap the distribution of the other species. Generally, there was a marked distinction between males and females of the same taxon whereby males, especially Gorilla and Pongo males, with larger canines were closer to the negative end of this axis than females. Differences between males and females on this axis also appeared to be driven to some extent by the more anterior mental foramina, relatively shorter dental arcades and more extensive anterior convergence of females. Extant Homo was an exception to this trend with tremendous overlap of the sexes indicative of minimal sexual dimorphism for the traits examined, including mental foramen A/P distance.
Variation on PC axis 2 was primarily driven by differences in relative mental foramen A/P distance and, to a lesser extent, dental arcade length relative to the geometric mean (Table 6). Pan and Gorilla specimens were mostly separated from one another along this axis. Gorilla males, particularly those of the eastern subspecies, were negatively projected on the second axis reflecting their anteriorly positioned mental foramina combined with relatively long dental arcades; Gorilla females and extant Homo also were closer to the negative end of this axis, the latter taxon likely because of its anteriorly placed mental foramen (Fig. 4). Pan, and to a lesser extent Pongo, with more posteriorly positioned mental foramina and relatively short dental arcades with respect to size, were projected closer to the positive extreme of PC axis 2.
Table 6. Principal component loadings of variables scaled by the geometric mean
PC Axis 1
PC Axis 2
Dental arcade length
Mental foramen position
Comparisons with Previous Studies
The results of this study indicate that the A/P position of the mental foramen significantly differentiates some extant hominoid species from others, rejecting the first null hypothesis. These results are similar to two early qualitative studies which cited Pan troglodytes as having more posteriorly positioned mental foramina than other great apes (Simonton, 1923; Montagu, 1954). The finding that the eastern subspecies of Gorilla gorilla exhibits more anteriorly placed mental foramina when compared with the other great apes differs from previous assessments of interspecific diversity in hominoids (e.g., Aitchison, 1965; Wood and Chamberlain, 1986; Brown, 1989). Females of the two eastern Gorilla gorilla subspecies are especially notable in how anteriorly positioned their mental foramina are. This may be because the quantitative approach we used is not directly comparable with the qualitative methods used to collect the nonmetric data, or because previous researchers relied primarily on G. g. gorilla specimens to represent the species, whereas our study included all three subspecies. Gorillas are more similar to other great apes in this trait when only the western subspecies is included in the analysis, because G. g. gorilla has more posteriorly positioned mental foramina than the other gorilla subspecies. This demonstrates the importance of sampling from as many geographically distinct populations as possible when comparing multiple species.
The antero/posterior position of the mental foramen was one of the characters used to separate gorillas into three subspecies (Vogel, 1961; Groves, 1970, 1986). Our study differs from earlier analyses of this character (Vogel, 1961; Groves, 1970, 1986; Goodall and Groves, 1977; Groves and Stott, 1979) in finding that variation among Gorilla gorilla subspecies is not clinal, but rather significantly differentiates the two eastern subspecies, with more anteriorly positioned mental foramina, from G. g. gorilla when the sexes are pooled. These results support recent genetic and morphological studies suggesting that the most significant split within Gorilla gorilla is between the eastern and western populations (Ruvolo et al., 1994; Garner and Ryder, 1996; Uchida, 1996, 1998; Groves, 2001; Taylor, 2002; Robinson, 2003; Taylor and Groves, 2003).
The A. africanus specimen, MLD 18, falls just outside the A. afarensis range of variation for mental foramen A/P position in having a more posteriorly positioned mental foramen. The difference between the two groups is similar to that between Pan paniscus and P. troglodytes. Previous analyses of mental foramen position in these taxa have not found a significant difference between them (Tobias, 1991; Robinson, 2003). However, as only one A. africanus mandible was included in this study, we cannot confidently reject the null hypothesis that these species have indistinguishable mental foramen A/P positions. These data do suggest that Australopithecus as a whole is more similar to Homo, and the two eastern Gorilla subspecies, and dissimilar to Pan for this character.
Taxonomic and Phylogenetic Implications
The A/P position of the mental foramen significantly differentiates extant hominoid species from one another, suggesting that this character is potentially informative for taxonomic studies of fossil hominoids. Whether and how it is used in phylogenetic analyses depends on the extent of its covariation with other traits. Three of these, dental arcade length, canine size, and anterior convergence, were explored here.
In the ANCOVA analyses, we found that mental foramen A/P distance scaled in a consistent manner with dental arcade length within hominoid species. In most hominoid taxa the A/P position of the mental foramen was significantly influenced by dental arcade length rejecting the first part of the third null hypothesis. In Pan troglodytes and eastern Gorilla subspecies, the null hypothesis of isometry for mental foramen A/P position relative to dental arcade length could not be rejected. For the other taxa, this relationship was positively allometric indicating that within each taxon (Homo sapiens, Pongo pygmaeus, Gorilla gorilla gorilla, and Pan paniscus), those individuals with longer dental arcades have more posteriorly positioned mental foramina. Homo sapiens is the only taxon to exhibit positive allometry of mental foramen A/P position when the sexes are analyzed separately, and unlike in the great apes, males and females are not clearly distinguished along the first principal components axis. This would appear to indicate that great ape species exhibit positive allometry because of sexual dimorphism in the A/P position of the mental foramen, with males having more posteriorly positioned mental foramina. Modern humans, on the other hand, exhibit positive allometry along a continuum from females to males and have minimal sexual dimorphism in mental foramen A/P position. Homosapiens is distinct from the great apes in its greater than expected anterior placement of the mental foramen with respect to dental arcade length regardless of whether sexes are examined separately or together.
Intraspecific variation in the A/P position of the mental foramen was also found to have been influenced by sexual dimorphism in canine size, rejecting the second part of the third null hypothesis. Thus, the size of the canine roots could also be important in influencing the position of the mental foramen. This is supported by the observation that those taxa that are most sexually dimorphic for canine size (i.e., Gorilla gorilla and Pongo pygmaeus) also exhibit the highest levels of sexual dimorphism for mental foramen A/P position. Homo sapiens, Pan paniscus, and all Pan troglodytes subspecies exhibit only limited dimorphism in canine and body size (Clutton-Brock et al. 1977; Plavcan and van Schaik, 1997b; Smith and Jungers, 1997; Plavcan, 2001), and are not significantly sexually dimorphic for mental foramen A/P position.
Large canine roots in males extend deeper into the mandibular corpus, and may restrict the mental foramen to a more posterior position in male gorillas and orangutans compared with females of these genera, although this seems unlikely given that the mental foramen ossifies before the development of the canine root, at least in humans (Scheuer and Black, 2000). Alternatively, dimorphism in mental foramen position may reflect a change in the length of the entire anterior tooth row, as increases in dental arcade length in males could be disproportionately expressed by increases in the anterior dentition.
There is also a developmental perspective to consider as the position of the mental foramen changes over the course of postnatal ontogeny. For example, in both humans and Neandertals, the mental foramen “migrates” posteriorly during postnatal development as the lower jaw lengthens during the eruption of the first and second molar (Williams and Krovitz, 2004). This displacement of the mental foramen during postnatal ontogeny may be an ancestral developmental pattern among hominoids and is largely taxon specific. It is possible that dietary stresses on the mandible during development could influence the posterior migration of the mental foramen and that some differences in adults may derive from distinct dietary life histories.
Unlike intraspecific variation, interspecific diversity among hominoids does not correspond well to differences in canine size. The taxa with the largest and smallest canines, eastern Gorilla gorilla and Homo sapiens, respectively, have the most anteriorly positioned mental foramina. Great ape taxa with longer dental arcades generally have more anteriorly positioned mental foramina. Thus, interspecific diversity among great apes could reflect increased growth of the posterior portion of the corpus relative to the anterior in the elongated mandibles of Pongo pygmaeus and especially Gorilla gorilla. Pan species exhibit greater anterior convergence than the larger great apes, which could also be related to their more posteriorly positioned mental foramina. Hominins have relatively anteriorly positioned mental foramina probably because infradentale is brought closer to mental foramen because of a reduction in the size of their anterior dentition concomitant with the emergence of a parabolic and anteriorly convergent dental arcade. These results suggest that phylogenetic analyses of hominoids should investigate the relationship between mental foramen A/P position, dental arcade length, mandibular shape indices, and canine size before using these traits as independent characters.
Contrary to some previous reports that intraspecific variation is too extensive for the A/P position of the mental foramen to be used to significantly differentiate extant hominoid species (Wood and Chamberlain, 1986; Brown, 1989), in this study some hominoid species could be separated from one another by the A/P position of mental foramen along the midline chord. Thus, this character has the potential to be useful in studies of fossil hominoid taxonomy and phylogeny. In general, those species with the longest dental arcades (i.e., Gorilla) had more anteriorly positioned mental foramina. Extant Homo is an exception to this pattern having anterior mental foramina despite its relatively and absolutely short dental arcades. Pan troglodytes is distinct in exhibiting a more posterior mental foramen than other great apes. Australopithecus afarensis is more similar to Homo sapiens than to the other extant taxa, and in the fossil hominins available the mental foramen was anteriorly positioned, possibly because of the reduction of the anterior dentition, which alters the shape of the hominin anterior dental arcade. The Australopithecus africanus mandible exhibited a more posteriorly positioned mental foramen than the A. afarensis specimens included in this study.
The finding that the mental foramen was significantly more anteriorly positioned in Gorilla gorilla than in other nonhuman hominoids differs from previous studies of this character. One possible reason for this disparity is the inclusion of all three gorilla subspecies in this analysis. Gorilla gorilla gorilla had substantially more posteriorly positioned mental foramina than other Gorilla subspecies. The disproportionate use of western lowland gorillas in studies of hominoid morphological diversity may have incorrectly led to the suggestion that gorillas are similar to other great apes for this character. This highlights the importance of examining as broad a range of popultions as possible when conducting interspecific comparisons of morphological features.
The significant relationships between mental foramen A/P distance and canine crown area, anterior convergence, and dental arcade length suggests that the A/P position of the mental foramen on the mandible is influenced by a number of traits. Covariance in these variables should be investigated in phylogenetic analyses before they are included as independent characters. Further studies exploring how the relative sizes of the anterior and posterior dentition influence mental foramen A/P position would likely improve our understanding of the causes of variation in this character.
CR would like to thank the curators and collections managers at the following museums for allowing access to their extant hominoid collections in their care: the American Museum of Natural History, the Museum of Comparative Zoology and Peabody Museum at Harvard University, the Anthropologische Staatssammlung and the Zoologische Staatssammlung in Munich, the British Museum of Natural History, the Musée Royal de l'Afrique Centrale, the National Museum of Natural History (Smithsonian), the Powell-Cotton Museum, the Nationaal Natuurhistorisch Museum, and the Zoologische Museum in Berlin. He would also like to thank Ato Muluneh Gebre Mariam and Ato Jara Haile Mariam at the National Museum of Ethiopia and Beverly Kramer and Kevin Kuykendall at the University of the Witwatersrand Medical School for allowing access to the fossil hominin material in their care. Tim White kindly permitted CR to examine the Maka mandibular specimens. Special thanks are given to William Kimbel and Donald Johanson for permitting CR to study the published and unpublished mandibles from Hadar. CR would also like to thank Terry Harrison, Michelle Singleton, Matt Carlton, Noah Stern, Fiona Bohane and Gary Sawyer for assistance with various aspects of this research. FW thanks Mike Sutherland for statistical assistance.