Affinities of Sm 3
Geometric morphometric analysis involved the collection of 3D coordinates of five midsagittal landmarks and a series of points between them. After conversion to 2D coordinates, the inter-landmark points were resampled to yield “lines” consisting of 50 semi-landmarks on each specimen; landmarks and lines were analyzed separately. The lines provided much greater detail given the higher number of coordinates, but the two analyses yielded basically similar results. The modern human specimens were clearly separated from the known fossils in a graphical superimposition based on Procrustes fitting of semi-landmarks as well as in both a principal components (PCA) of the aligned Procrustes coordinates and a canonical discriminant (CDA) analysis of the PCA scores. The two “archaic Homo sapiens” specimens are not clearly distinguishable in either analysis from the Homo erectus range in the sagittal profile. Sm 3 fell between the fossil and modern groups in the Procrustes aligned image (Fig. 2) and also in the PCA (Fig. 3) and CDA (Fig. 4), where it was closer to the fossils, and especially to those from Ngandong in the CDA. When treated as an unknown in the DA, Sm 3 was classified as H. erectus, while two of the known H. erectus were misclassified as “archaic H. sapiens”. When the DA was applied to landmark data, Sm 3 was classified as “archaic H. sapiens”, along with three of the H. erectus. A minimum spanning tree derived from the semi-landmark Procrustes distances (Fig. 5) placed Sm 3 between the two fossil groups, distant from the modern humans. A permutation test on these distances (Table 3) suggested that Sm 3 (and also H. erectus) could potentially be included with the “archaic H. sapiens” sample, but when a Bonferroni correction is applied, the distance between Sm 3 and H. erectus falls below significance; thus, the three fossil groups are not statistically distinguishable by this test. In sum, Sm 3 falls within the range of variation of the studied Homo erectus sample (see Fig. 2b), which is not readily distinguishable from “archaic H. sapiens”. On the other hand, it is the individual most similar in shape to anatomically modern humans, especially in the frontal region, in its sagittal profile.
The comparative morphological analysis involved visual comparison of casts, with reference to various cited publications. Again, Sm 3 is most similar overall to Indonesian representatives of Homo erectus, especially those from Ngandong and Sambungmacan.
In frontal bone morphology, the supraorbital torus is gracile and most similar to those of female specimens, such as Ngandong 7. The midline supratoral plane is steeper vertically and glabella projects less anteriorly in Sm 3 than in any of the other H. erectus fossils examined here. The supratoral region of Sm 3 is most similar to the Ngandong specimens in that it shows no sulcus and its plane is straight above glabella but concave above the trigones. The postorbital constriction of Sm 3 (see Fig. 6) is closest to that of Indonesian fossils: Ngandong, Sm 1, and Ngawi. The upper portion of the frontal squama in Sm 3 is more rounded than in the Indonesian and most African (or European) fossils examined, but it is similar to those from Zhoukoudian and to ER 3733. Although these latter specimens are superficially similar to Sm 3 in this respect, they show a much stronger frontal keeling which greatly contributes to the rounded shape of their frontal squama in lateral view. The pattern of sagittal keeling on the frontal and anterior parietal in Sm 3 is distinctive: weak on the frontal but stronger on the parietal, without effect on the frontal squama rounding, and no bregmatic eminence or coronal ridging. This is most similar to Sm 1, less so to Sangiran 2 and 17.
Although an angular torus has long been considered a characteristic of Homo erectus, none is visible on Sm 3, which instead presents only a slight swelling. In fact, the occurrence of the torus is variable in several studied samples: Sangiran, Ngandong, Zhoukoudian, East Africa, and Sambungmacan. The tympanomastoid fissure between the mastoid process and the tympanic, another feature typical of Asian H. erectus, is well developed in Sm 3 and most similar to those from Ngandong (see Fig. 7). Other Asian fossils present a weaker fissure with a different shape, while most of the African specimens lack it. The presence of a Ngandong-like fissure in WT 15000 may oppose the distinction between African and Asian populations based on this feature (or may be age-related). The squamotympanic fissure in Sm 3 runs in the deepest portion of the deep and antero-posteriorly short mandibular fossa, as in all other Indonesian fossils and OH 9.
The supramastoid crest of Sm 3 courses upward at an angle to the suprameatal crest to cross the squamosal suture above the parietal incisure. It is separated completely from the mastoid crest by a wide and shallow supramastoid sulcus. This pattern is matched in the Ngandong fossils and in Sm 1 and Sgr 4, but differs in Zhoukoudian, Sgr 2 and 17, the African specimens, and “archaic Homo sapiens”. On the other hand, the prominence of the suprameatal and supramastoid crests in Sm 3 is most similar to that of Zhoukoudian, Sangiran 17, and Sm 1. The crests are weak in the African specimens (including Kabwe), while Ngandong is variable in this feature.
The occipital torus of Sm 3 is rather robust and thick supero-inferiorly, much as in Ngandong 7. The superior margin of the central region is arched as in Sm 1 and the Ngandong series, rather than straight as seen in most other H. erectus fossils. The nuchal scale in Sm 3 is moderately excavated for muscular attachment, and an external occipital crest is visible. This region is less well developed than in the Ngandong series or Sm 1, but more so than in the Sangiran, Zhoukoudian, or African fossils. The greatest similarity of Sm 3 in the occipital torus area is to Sm 1 and Ngandong 7, although the angle between its nuchal and occipital scales is less acute than in any of the fossils observed. In the region of the foramen magnum (see Fig. 8), Sm 3 appears to present both a postcondyloid tuberosity and an opisthionic recess, although breakage renders these observations questionable. The preserved morphology is closest to that seen in the Ngandong sample.
In sum, both the geometric morphometric, and comparative morphological analyses link Sm 3 most closely with the Ngandong sample and Sm 1, with other Indonesian fossils such as Trinil 2 and those from Sangiran also being generally similar. The Zhoukoudian sample and the several African Homo erectus examined were usually different morphologically from Sm 3, although ZKD and ER 3733 showed similarity to it in the curvature of the upper frontal scale. Both “archaic Homo sapiens” fossils examined and the two samples of modern humans differed consistently from Sm 3 and (except in the sagittal profile morphometrics) from most H. erectus fossils. In two areas, Sm 3 was quite distinctive among all the fossils studied. On the lower frontal, the supratoral plane is more vertical and the glabella more anteriorly projecting than any fossil, although it did not closely approach the shape seen in modern humans. The occipital angle is less acute than in the fossils examined.
Overall, there would appear to be no strong reason not to include Sm 3 as a member of Homo erectus, especially when that taxon is broadly interpreted to include African representatives. It is morphologically distinctive in the lower frontal and mid-occipital regions but in general falls well within the range of variation of Homo erectus in both analyses. Those distinctions, however, are broadly “in the direction” of modern humans in that they represent an “unrolling” of the neurocranium both anteriorly and posteriorly. In the geometric morphometric visualizations, Sm 3 was consistently placed between the other fossils and modern humans as well. What is the evolutionary meaning of this intermediacy?
Currently, there are two major models of the origin of modern humans: regional continuity and single-region dispersal (see, e.g., Tattersall and Delson, 2000; Stringer, 2000; Thorne, 2000). The former envisions H. erectus (termed early H. sapiens by its leading proponents) as evolving into modern H. sapiens in various Old World regions in parallel, with migrational gene flow serving to link all populations at any given time. Under such a model, the apparently more modern morphology of Sm 3 among known Indonesian H. erectus might be interpreted as documenting such in situ evolution. But there is no evidence that the morphology of Sm 3 was typical of the biological population of which it was part; it might have been just a variant individual which (perhaps in part as a result of small body size) shared superficial similarity with later humans. Paleontologists must usually assume that any unique individual discovered was representative of the biological population in which it lived, but with the recovery of additional specimens (e.g., OH 5 is probably an extreme member of the taxon to which it belong as holotype), this is sometimes later shown to be untrue. The geographically closest individual, Sm 1, shared a number of features with Sm 3, but certainly not its most distinctive aspects. In fact, there is no way at present to choose among these three possible scenarios: 1.) Sm 3 was a representative of a population of H. erectus evolving in the direction of modern humans; 2.) Sm 3 was a representative of a morphologically distinctive population of Indonesian H. erectus which later merged with more “typical” forms or died out, not leading to any specific later group—most of the authors prefer this alternative—or 3.) Sm 3 was a distinctive individual among “typical” Indonesian H. erectus. Further specimens from the Sambungmacan area might resolve this uncertainty, but only if they share the novel features of Sm 3.
As noted by Márquez et al. (2001), among many others, has noted, the identification of sex in human fossils is a probabilistic activity. Features such as relative robusticity can only be safely utilized when a sample is available within which relativity can be assessed. Here, one is dealing with a single individual specimen which has been referred to a taxon characterized by a higher overall degree of robusticity than in modern humans, which renders the uncertainty even greater. Nonetheless, there is a broad consistency of admittedly weak indicators which point to Sm 3 having been a female.
In the geometric morphometrics, the centroid size (CS) of Sm 3 is the smallest of any fossil, falling between the smallest modern human and ER 3733 (generally viewed as female). In the principal component analysis (PCA) of the semi-landmarks, ANOVAs revealed a marginally significant sex effect for PC1 and a more significant one for PC4; the position of Sm 3 appears weakly to suggest a female identification. In terms of morphology, the gracility of its supraorbital torus and of its sagittal and coronal ridging also seem to indicate female sex. The lack of an angular torus in Sm 3 is another potential indicator of female sex, but as noted above, the putatively female ZKD 11 has a stronger torus than the supposed male ZKD 12. On the other hand, the strong supramastoid crest in Sm 3 would be expected in a male rather than female individual. Moreover, Santa Luca (1980) has discussed how Homo erectus “females” (as estimated from overall size) seem to present more keeling but less development of other “superstructures” (angular, occipital, and supraorbital tori; supramastoid and other crests) than males. The mosaic seen in Sm 3, of relatively gracile to nonexistent tori and circum-bregmatic ridging, combined with small size, does not correspond to either pattern observed by Santa Luca, but that may only reflect the situation in Ngandong. Given the patterns of sexual dimorphism represented by the Ngandong sample (male 12 and 6 vs. female 7 and 1), Sangiran (male 17 and 4 vs. female 2), Zhoukoudian (male 12 vs. female 11), and East Africa (male OH 9 [and WT 15000] vs. female ER 3733 and 3883), the Sambungmacan fossils could also represent a dimorphic duo.
Contributions of Geometric Morphometrics
As has been discussed by many authors (e.g., Rohlf and Marcus, 1993), geometric morphometrics is “superior” to traditional or inter-landmark morphometrics in that it preserves the interrelationships of all landmarks and the surfaces between them. This study is one of the first (in paleoanthropology at least) to analyze coordinates from lines connecting several landmarks (see also Bookstein et al., 1999; Dean et al., 1996) and the first to apply these methods to determine the affinities of a newly recovered fossil hominin. The several statistical tests applied here represent some of the ways in which geometric morphometric data can be examined to yield phenetic estimates of the evolutionary relationships (and sex) of individuals, samples, and taxa. The intermediate position of Sm 3 indicated by the graphical superimposition as well as the multivariate techniques is not clearly revealed by the comparative morphological examination of the same specimen or specimens. Indeed, both the distinctive frontal elevation and the more “open” occipital angle were observed in the graphical Procrustes analysis before being confirmed by the morphological study. One weakness of this morphometric work is its confinement to the 2D analysis of features in the sagittal plane, but that limitation will be exceeded through continued advances in this field. Our research group is also seeking ways to combine these continuous-variable methods with the coded discontinuous approach required for numerical cladistic analysis (see also, e.g., Naylor, 1996; Thiele, 1993; Zeitoun, 2000).
An unexpected result of this geometric morphometric analysis is the finding that the Procrustes-aligned profiles of modern and extinct samples crossed near lambda and (less clearly) bregma, which might imply that the growing margins of the parietal (and other bones?) constrain the location of evolutionary change in cranial shape. This type of graphical observation could not have been discerned using other forms of analysis.