Australia: The Land Where Time Began

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Dmanisi, Georgia, A Complete Skull, and the Evolutionary Biology of Early Homo

An impressive sample of cranial and postcranial remains have been recovered from the site of Dmanisi in Georgia (the country) which demonstrate that Homo was present outside Africa around 1,8 Ma. In this paper Lordkipanidze et al. present a new cranium from Dmanisi (D4500) that, together with its mandible (D2600), represents the first known completely preserved adult hominid skull from the Early Pleistocene.  A small braincase (546 cc) with a large prognostic face represents close morphological affinities with the earliest known Homo fossils from Africa. Direct evidence for wide morphological variation within and among early homo palaeodemes is provided by the Dmanisi sample, which now comprises 5 crania. The existence of a single evolving lineage of early Homo, with physiographic continuity across continents is implied by this. Hominid fossils, a rich vertebrate fauna and Mode I (Oldowan) stone artefacts that co-occurred in geological and taphonomic contexts that were well understood, were uncovered by excavations at Dmanisi, Georgia. A short time after 1.85 million years ago (Ma) occupation of the site began and is documented until 1.77 Ma (Gabunia et al., 2000; Vekua et al., 2002; Lordkipanidze et al., 2005; Lordkipanidze et al., 2006; Lordkipanidze et al., 2007; Ferring et al., 2011  ). The preservation, as well as the temporal and geographic setting of at least 5 hominid individuals make Dmanisi a site that is crucial in understanding the variation patterns, biogeography, and evolution within emergent Homo. The Dmanisi sample is linked to the largely contemporaneous fossils from Africa that have been attributed to H. habilis and/or H. erectus, by the generalised (primitive) craniomandibular morphology, small cranial capacity, moderate body size and a mosaic of primitive and derived postcranial features. It is indicated there are affinities to H. erectus in East Asia by various features of the cranial vault and base (Lordkipanidze et al., 2006; Lordkipanidze et al., 2007; Rightmire, Lordkipanidze & Vekua; 2006; Rightmire & Lordkipanidze, 2010).

In this paper Lordkipanidze et al. present a complete cranium that expands the range substantially of variation that is observed in the Dmanisi sample, with implications of earl history of the genus Homo. In 2005 the specimen D4500 was recovered from layer B1y in Block 2 of the Dmanisi excavation area (Supplementary materials available on Science Online). The same individual as mandible D2600 is represented by D4500, which was found 5 years earlier (Gabunia et al., 2002). The association of D4500 and D2600 (“skull 5”) constitutes the most complete adult skull that is known from Homo in the Pleistocene (“early Homo”; the definition of Pleistocene follows the new terminology). According to Lordkipanidze et al. skull 5 is probably associated with the postcranial material of an adult individual that has body proportions that are almost human [(Lordkipanidze et al., 2007); supplementary text S1 and Fig. S1)]. It is now possible to document the morphology of an entire cranium with its associated mandible and teeth and to study anatomy that has not previously been known for early Homo, as skull 5 is intact and free from taphonomic deformation.

Cranium D4500 – description

As the result of a small braincase with a large prognathic face the morphology of skull 5 stands apart from any other known specimen of fossil Homo.

Braincase

The endocrinal volume (ECV) that was evaluated from computed tomography (CT) data is 546 ± 5 cm³. The braincase, coupled with its small ECV the braincase is low, though comparatively wide and basically elongate. The frontal squama is moderately sloping. The parietals are bossed, exhibiting only a slight midline keeling in their posterior half. The zygomatic arches are massive, and spacious temporal fossae indicate voluminous masticatory muscles. Temporal lines are well separated from each other (minimum from cranial midplane 12 mm behind bregma: 20 mm).Prominent supramastoid crests are exhibited by the temporal bone and porial saddles which give the neurocranium a squat, bell-like shape when viewed from the rear.

There is a marked protuberance on the occipital bone immediately below its lambdoid margin, which extends across the midplane by ~30 mm on either side. The prominence of this “lambdoid bump,” together with a massive protruding inion, lends the upper occipital plane an almost vertical orientation, whereas the nuchal plane is inclined only moderately (21^o), relative to the Frankfurt horizontal (FH) plane. The occipital transverse torus in ruggedly built and the nuchal region is deeply sculpted. A strong nuchal ligament is suggested by a bilaminar link that links the inion with the opisthion. The mastoid processes are large and steeply inclined medially. Their inferior portion is compressed mediolaterally to form a distinctive flange-like structure that extends posteriorly. Overall, cranial superstructures of D4500 are massive and more prominent than those in other Dmanisi individuals, which suggests it represents a male.

Temporal bones and cranial bones

The right zygomatic arch exhibits in vivo deformation which indicates a healed though displaced multiple fracture behind the masseteric origin. The left temporomandibular joint (TMJ) as well as the left mandibular condylar bar evidence for degenerative arthritic deformation. The left TMJ and the right zygomatic arch are unaffected by pathology. There is marked lateral extension of the TMJ with 61% of the glenoid fossa beyond the external wall of the vault, below the zygomatic shelf. The fossa itself is shallow, transversely oriented (tympanomedian angle 3^o), and has a low anterior wall that merges smoothly with the preglenoid planum. The tympanic plate is massive and exhibits a prominent vaginal process. Medially the tympanic is expanded to form a robust supratubarius process. The petrous pyramid closely approaches the wall of the basioccipital, thus reducing the foramen lacerum to a crevice. The main axis of the pyramid forms an angle of 34^o (petromedian angle) with the midsaggital plane. The foramen magnum is oval in shape and level (inclination 0^o) with respect to the FH. Basicranial flexion, as measured by the orientation of the clival plane relative to the sphenoid plane, is low (128^o).

Face

The face of skull 5 is among the largest and most prognathic known from early Homo, which contrasts with the small brain. The glabellar region is massive and substantially overhangs the mid-face. The orbits are overarched by thick bar-like tori; a shallow post-torus shelf (rather than a sulcus) extends posteriorly towards the frontal squama. Post orbital constriction is marked. The zygomatic processes of the maxillae are massive and laterally flaring. The anterior surface is vertically oriented and coincides with the orbital plane, thus forming a zygomatic-orbital plane. As a consequence of the tall and wide midface, the zygomatic-alveolar crests are markedly angled. The roots of the zygomatic processes originate between the first and second molars. The nasal floor is delimited anteriorly by a smooth (rather than sharply angled) sill. The inclination of the nasal-alveolar clivus relative to the alveolar plane is 42^o. The subnasal portion of the clivus is slightly concave, whereas its alveolar portion is convex, covering the large incisor roots. The palate is long and arched; the incisive foramen is located at the position of the second premolar (P⁴), indicating marked prognathism of the maxilla and anterior dentition.

Dentition

The upper and lower dentition of skull 5is heavily worn, and crown morphologies are only partially preserved. Estimated molar dimensions are comparatively large, the maxillary as well as mandibular molar sizes increase from M1 to M3. Judging from root orientation, the maxillary incisors were strikingly procumbent. The open bite (structural non-occlusion of the incisors), rounded labial wear surfaces on upper incisors and rounded lingual wear surfaces on lower incisors, respectively, and labiolinguallly oriented striations on these surfaces suggest that the anterior dentition was used in paramasticatory activities such as gripping (Lozano et al., 2008). The first maxillary premolars (P³) are situated posteriorly to Cs, such as massive C/P³ juga square off the front of the maxilla. Similarly massive C/P³ juga are present in the mandible D2600 (Gabunia et al., 2002). P³s have 3 roots; P⁴s are double rooted; with the buccal root exhibiting 2 canals (3 rooted P³s and double rooted P⁴s have also been reported for other Homo specimens. The P₃s of mandible D2600 have 2 roots (the distal roots and 3 canals (Walker & Leakey, Eds., 1993). The P₄s are not preserved.

Comparative analysis

According to Lordkipanidze et al., skull 5 was the first complete specimen that provided evidence of how the face (including the mandible) of adult early Homo was oriented and positioned relative to the braincase. Prior to the discovery of skull 5 completely craniomandibular morphology of early Homo was 2 adolescents, whose facial skeletons were not fully developed (KNM-WT 15000 and D2700/D2735) (Vekua et al., 2002; Walker & Leakey, Eds., 1993), and the Dmanisi individual that was senile D3444/D3900, the gnathic morphology of which was modified strongly by alveolar bone resorption after tooth loss (Lordkipanidze et al., 2005; Lordkipanidze et al., 2005). Anatomical connections between preserved neurocranial and maxillofacial parts among adult early Homo specimens from Africa and East Asia are typically incomplete and facial to neurocranial orientation have remained a matter of debate (Bromage et al., 2008; Leakey et al., 2012). Therefore the current perception of skull morphology of early Homo is influenced strongly by adolescent representatives (and the less complete and taphonomically distorted adult cranium KNM-ER 1813) that exhibit comparatively orthognathic faces with superstructures that are lightly built. It is now indicated by skull 5 that small-brain large-faced, remarkably prognathic and robust morphologies are all within the normal range of early Homo. The smallest of the Dmanisi sample (skulls 1 to 4: 601 to 730 cm³) is represented by skull 5 (546 cm³), and it is at the lower end of the variation of the H. habilis hypodigm [509 to 687 cm³ (Holloway et al., 2004; Rightmire, 2004)]. This individual is placed within the range of variation that has been estimated for early Homo and at the lower end of variation of African H. erectus and modern humans (Holliday, 2012), by the stature and body mass estimates that were obtained from the postcranial elements that are probably associated with skull 5 [146 to 166 cm, 47 to 50 Kg (Lordkipanidze et al., 2007). The skull 5 individual has provided the first evidence that early Homo comprised adult individuals with small brains, though with body mass, stature and limb proportions reaching the lower range limit of modern human variation (Lordkipanidze et al., 2011; Holliday, 2012). The encephalisation quotient (EQ) of the skull 5 individual was estimated as ~2.4, which is within the range of variation for Australopithecus (Holloway, Broadfield & Yuan, 2004. Lordkipanidze et al. suggest the larger ECV of early Homo as compared to Australopithecus africanus [340 to 515 cc (Holloway, Broadfield & Yuan, 2004)] and Au. Sediba [420 cc (Holliday, 2012)] might therefore reflect primarily an evolutionary increase in body size rather than increased encephalisation.

Skull 5 has allowed the scope of comparisons to be widened, though previously similarities between Dmanisi and eastern African fossils that were attributed to H. ergaster and H. erectus have been documented (Lordkipanidze et al., 2006; Rightmire, Lordkipanidze & Vekua, 2006; Rightmire & Lordkipanidze, 2010; Gabunia et al., 2002; Baab, 2008). Skull 5 exhibits midfacial architecture which has morphological affinities with contemporaneous African specimens SK 847 and OH 65 (Blumenschine et al., 2003), as well as with early representatives of Homo in eastern Africa such as KNM-ER 1470 and KNM-ER 62000 that dates to ~ 2.0 to 1.9 Ma (Leakey et al., 2012). The naso-alveolar is moderately sloping and laterally wide curving around the buccal roots of P³s, in all these specimens.

The Chemeron temporal fragment, which dated to 2.4 Ma, that was suggested to be the earliest fossil evidence of Homo (Hill et al., 1992; Sherwood, Ward & Hill, 2002), though this assignment has remained inconclusive given the wide variation in TMJ position and morphology in the Dmanisi and early Homo samples. The maxilla of skull 5 is, however, similar in overall form and dento-alveolar features to the well-preserved early Homo maxilla A.L. 666-1 from Hadar, Ethiopia, with a geological age of 2.3 Ma (Kimbel, Johnson & Rak, 1997). Recently, the generic and chronological status of A.L. 666-1 has been questioned, and it has been proposed that A. Sediba (1.977 Ma) is instead, a potential ancestor of the Homo lineage (Pickering et al., 2011). Such a scenario has, however, been falsified by the close morphological affinities between A.L. 666-1, additional early Homo specimens from eastern Africa such as OH 65 and KNM-ER 1470, and now skull 5.

It has now been established by the enlarged sample of Dmanisi variation is crucial to identifying patterns of variation among and between palaeospecies of early Homo. Evidence has been provided by several studies for variation along and across a single evolving lineage of early Homo (Asfaw et al., 2002; Suwa et al., 2007), with differences between fossil specimens reflecting, primarily, intraspecific variation at a population level and evolutionary change within a species over time. However, other studies interpret variation in small samples of early Homo from Africa as reflecting taxonomic species diversity (Leakey et al., 2012; Wood, 1991; Wood, 1992; Spoor et al., 2007) and posit 3 or more largely contemporary palaeospecies (H. rudolfensis, H. habilis & H. erectus). According to this interpretation differences among individual fossil specimens indicate that there are interspecific differences and concomitant phyletic diversification. Information Variation within palaeodemes is depended upon for testing these contrasting hypotheses i.e., within populations of fossil species at a given point in space         and time (Howell, 1999). It is likely that a fossil sample represents a palaeodeme if 2 conditions are met. It must come from a stratigraphic and taphonomic setting [which is the case for Dmanisi (Lordkipanidze, et al., 2006; Lordkipanidze et al., 2007] that is spatially and temporally constrained, and it must be within-sample variation that is similar in range and mode to be within-deme variation in extant species that are closely related.

It is shown by geometric morphometric analysis and resampling statistics that shape of craniomandibular variation among hominids from Dmanisi is congruent with patterns and ranges of variation in chimpanzee and bonobo demes (Pan troglodytes, P. t. verus, P. t. schweinfurthii, and Pan paniscus and in a global sample of H. sapiens. Variation in cranial shape in all groups is mainly due to interindividual differences in size and orientation of the face relative to the braincase. The Dmanisi sample, which includes skull 5, therefore represents normal within-deme variation, which ranges from small-faced relatively orthognathic (typically female and/or subadult) individuals, to large-faced relatively prognathic individuals that are typically male.

It is also indicated by nonmetric cranial characters that there is substantial within-deme variation, and wider than typically recognised. Variation in maxillofacial features is shown the Dmanisi palaeodemes, which have been interpreted as evidence for taxonomic diversity in fossils from eastern Africa (Leakey et al., 2012; Spoor et al., 2007).

The best current available example of cranial form and form variation within the early Homo lineage is represented by the Dmanisi sample. It can tentatively be characterised as follows:

·        Face with flaring, vertically oriented zygomatic processes that are coplanar with the orbital plane;

·        Similar upper and midface widths;

·        Markedly angled zymaticoalveolar crests;

·        Marked alveolar prognathism;

·        C roots that exhibit parallel orientation relative to the cranial midplane;

·        naso-alveolar clivus sloping moderately and delimited laterally by C and/or P³ juga and;

·        ECV greater than ~500 cc.  

According to Lordkipanidze et al. these features from early Homo from nonrobust species of Australopithecus;

·       which exhibit a more protruding though less sloping naso-alveolar clivus;

·       inclined maxillary zygomatic processes;

·       moderately curved zygomaticoalveolar crests and;

·       superomedially tapering canine juga, which delimit laterally the anterior surface of the maxilla.

In early Homo other features, such as 3-rooted premolars, marked postorbital narrowing, a shallow glenoid fossa, and a moderate degree of Basicranial flexion, represent pleisomorphic (primitive character states that are shared variably with the Australopithecus species.

Discussion

Recognising diversity of species, as has been noted, comes at the expense of “admitting much variation” within species [(Darwin, 1869), p.51). Dmanisi adds to the growing evidence, together with data from Au. Afarensis, palaeodemes, such as A.L. 333 (White & Johnson, 1989;  Reno et al., 2003; Behrensmeyer, 2008), that variation in intrademic and intraspecific in the Plio-Pleistocene fossil hominids tends to be misinterpreted as species diversity, especially in the case of single fossil specimens from different localities are compared with each other (Gilbert, White & Asfaw, 2003). It is indicated by skull 5 and the other 4 Dmanisi specimens that cranial shape variation within early Homo populations was similar in mode to that seen in modern Pan demes. Also, it is indicated by Dmanisi that a proportion of character state variation in nonmetric features is a reflection of intrademic variation rather than real diversity of species. There are several implications of these findings for the interpretations of morphological diversity in the fossil record of early Home. Morphological diversity, when seen from the perspective of Dmanisi, in the African fossil Homo record about 1.8 Ma is probably a reflection of variation between demes of a single evolving lineage, which is appropriately named H. erectus. It appears that the hypothesis of multiple independent lineages (palaeospecies) (Leakey et al., 2012; Spoor et al., 2007) is less parsimonious, especially when there is no empirical evidence for adaptations to separate ecological niches. A classificatory, though not an evolutionary dilemma is raised by the hypothesis of phyletic evolution within a single polymorphic lineage, and it is premature to describe the rate(s) of evolution in this lineage, given the small sample that is available. Specimens that were previously attributed to H. ergaster are therefore sensibly classified as a chronosubspecies of H. erectus. Lordkipanidze et al. suggest it is probable that the Dmanisi population from the Early Pleistocene of H. erectus lineages from Africa, so it is sensibly placed within H. e. ergaster and formally designated as H. e. e. georgicus in order to denote the geographical location of this deme [therefore retracting the species status given earlier to mandible D2600 (Gabounia et al., 2002 [Gabunia?]).

Questions of early fossil Homo phylogenetics and classification remain to be resolved, given the scattered and fragmentary fossil record in Africa that predates Dmanisi. It has yet to be tested whether all of the fossils that are currently allocated to the taxa H. habilis and H. rudolfensis are actually part of the single evolving lineage of Homo. There are alternative scenarios, though Lordkipanidze et al. regard this null hypothesis to be parsimonious and fully compatible with new evidence from Dmanisi. At present there is no convincing signature of early Homo cladogenesis, given the range of variation that is observed in the Dmanisi palaeodeme. Increase in brain size and correlated changes in the craniofacial morphology within the evolving lineage of H. erectus are exhibited by the fossils from Africa that postdate the Dmanisi ensemble. It is, moreover, likely that the underpinning of the East African dispersal of H. erectus, as well as the roots of the subsequent evolution of H. erectus in Africa (e.g., OH 9, Daka), shared greater craniofacial robusticity.

The strong African affinities that were recognised previously for this early Eurasian outpost of the Homo genus is reinforced by the new evidence from the ancient Dmanisi deme of early Homo (Rightmire, Lordkipanidze & Vekua, 2006). Variation between continents may therefore provide insight into the evolutionary population dynamics of early Homo. That genetic and phenetic variation decreases with geographic distance from Africa is well known from the dispersal in the Upper Pleistocene of modern humans from Africa due to serial founder effects as well as population bottlenecks. Modern human phenetic variation in western and eastern Asia is 85 and 95% of African variation, respectively, e.g. (Manica et al., 2007). Direct comparisons must remain tentative as the expansion of early Homo from Africa might have occurred at longer time scales. The observation that Dmanisi conserves a substantial proportion of cranial shape and its variation among early Homo from Africa, nevertheless, speaks for genetic continuity. The effective size of early Homo in western Asia might have been similar [N_e >10,000 (Marques-Bonet, Ryder & Eichler, 2009)], as intrademic variation in Dmanisi is similar to that found in extant and extinct near relatives. Also, the early H. erectus from Java (Trinil/Sangiran) (Kaifu et al., 2005; Kaifu et al., 2010), the dentognathic remains of which are remarkably large and robust, exhibit close affinities with skull 5. Evidence is provided by this for morphological (and presumably underpinning genetic) continuity across large geographic distances, and for preservation in East Asia of an appreciable proportion of the variation that was originally present in palaeodemes of early Homo in Africa.

In contrast with continuity of early Homo across continents, current palaeontological data indicate a low degree of similarity between contemporaneous mammalian genera in Africa and at Dmanisi (Lordkipanidze et al., 2007), which implies a generally low rate of faunal exchange between Africa and Asia before about 1.8 Ma (Agustí & Lordkipanidze, 2011). The populational, ecological and evolutionary dynamics of early Homo probably differed significantly from those of coeval large mammals, which included other hominid lineages, as has been suggested earlier (Antón & Swisher, 2004). It is indicated by theoretical considerations that the long-range rate of dispersal of a population depends mainly on reproduction rates and habitat expansion (Hastings, 1996) and that intragroup cooperation can have an important role in population persistence (Hamilton et al., 2009). Various features such as:

·         Derived lower limb and foot morphologies (Lordkipanidze et al., 2007; Pontzer et al., 2010),

·         Tool mediated widening of the dietary niche towards meat eating (Lordkipanidze et al., 2006; Ferring et al., 2011) and,

·        increased levels of intragroup cooperation (Lordkipanidze et al., 2005),

might have led to increased levels of reproduction, survival, and mobility in early Homo and consequently the establishment of stable populations outside Africa. It is now indicated by skull 5 and other members of the Dmanisi palaeodeme that early Homo expanded from Africa to ultimately establish substantial populations in western Asia. This earliest hominid dispersal predated any significant increase in brain size. In order to test and modify the attendant hypotheses further analyses will be required. Ultimately, the identification of hominid palaeodemes and assessing within-deme variation (Howell, 1999) will be key to understanding mechanisms of evolution and geographic dispersal of early Homo.

Lordkipanidze, D., et al. (2013). "A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early <em>Homo</em>." Science 342(6156): 326-331.