Ardipithecus ramidus and the evolution of the human cranial base

Abstract

The early Pliocene African hominoid Ardipithecus ramidus was diagnosed as a having a unique phylogenetic relationship with the Australopithecus + Homo clade based on nonhoning canine teeth, a foreshortened cranial base, and postcranial characters related to facultative bipedality. However, pedal and pelvic traits indicating substantial arboreality have raised arguments that this taxon may instead be an example of parallel evolution of human-like traits among apes around the time of the chimpanzee-human split. Here we investigated the basicranial morphology of Ar. ramidus for additional clues to its phylogenetic position with reference to African apes, humans, and Australopithecus. Besides a relatively anterior foramen magnum, humans differ from apes in the lateral shift of the carotid foramina, mediolateral abbreviation of the lateral tympanic, and a shortened, trapezoidal basioccipital element. These traits reflect a relative broadening of the central basicranium, a derived condition associated with changes in tympanic shape and the extent of its contact with the petrous. Ar. ramidus shares with Australopithecus each of these human-like modifications. We used the preserved morphology of ARA-VP 1/500 to estimate the missing basicranial length, drawing on consistent proportional relationships in apes and humans. Ar. ramidus is confirmed to have a relatively short basicranium, as in Australopithecus and Homo. Reorganization of the central cranial base is among the earliest morphological markers of the Ardipithecus + Australopithecus + Homo clade.

Keywords: fossil record; human origins; occipital bone; skull; temporal bone.

Fig. 1.

Basal view of Ar. ramidus cranium ARA-VP 1/500. Dotted line indicates midline. cf, carotid foramen; ba, basion, the midline point on the anterior margin of foramen magnum. At natural size, the distance between the centers of the carotid foramina is 50.3 cm.

Fig. 2.

Box-and-whisker plot of relative bicarotid breadth. Horizontal line within box is the median; lower and upper ends of the box represent the first and third quartiles, respectively; and the ends of the whiskers represent ±1.5 × interquartile range. x-axis abbreviations: HsF, Homo sapiens female (n = 10); HsM, Homo sapiens male (n = 10); GgF, Gorilla gorilla female (n = 10); PtF, Pan troglodytes female (n = 10); PtM, Pan troglodytes male (n = 10); PpF, Pan paniscus female (n = 17); PpM, Pan paniscus, male (n = 12). Individual fossil specimen and comparative sample data are provided in Dataset S1.

Fig. 3.

Box-and-whisker plot of relative tympanic length. See Fig. 2 legend for explanation.

Fig. 4.

Anatomy of the tympanic/petrous relationship Pan, Homo, and Australopithecus: (A) chimpanzee, (B) modern human, (C) Australopithecus africanus (Sts 5), (D) Australopithcus robustus (DNH 7). See additional specimens in Fig. S2.

Fig. 5.

Anatomy of the tympanic/petrous relationship: Ardipithecus ramidus specimen ARA-VP 1/500, image reversed for ease of comparison with Fig. 4. Note tip of eustachian process is darkened by abrasion of surface bone.

Fig. 6.

Box-and-whisker plot of relative length of the external basicranium. Then range of estimated values for ARA-VP 1/500 is shown at left (main text and SI Text, Note 3). See Fig. 2 legend for explanation.

Fig. 7.

Comparison of basioccipital morphology in (A) Ardipithecus ramidus, ARA-VP 1/500; (B) Australopithecus afarensis, A.L. 417–1c; and (C) chimpanzee. ba, basion; bos, basioccipital synchondrosis; hc, hypoglossal canal.