Early origin for human-like precision grasping: a comparative study of pollical distal phalanges in fossil hominins

Abstract

Background: The morphology of human pollical distal phalanges (PDP) closely reflects the adaptation of human hands for refined precision grip with pad-to-pad contact. The presence of these precision grip-related traits in the PDP of fossil hominins has been related to human-like hand proportions (i.e. short hands with a long thumb) enabling the thumb and finger pads to contact. Although this has been traditionally linked to the appearance of stone tool-making, the alternative hypothesis of an earlier origin--related to the freeing of the hands thanks to the advent of terrestrial bipedalism--is also possible given the human-like intrinsic hand proportion found in australopiths.

Methodology/principal findings: We perform morphofunctional and morphometric (bivariate and multivariate) analyses of most available hominin pollical distal phalanges, including Orrorin, Australopithecus, Paranthropous and fossil Homo, in order to investigate their morphological affinities. Our results indicate that the thumb morphology of the early biped Orrorin is more human-like than that of australopiths, in spite of its ancient chronology (ca. 6 Ma). Moreover, Orrorin already displays typical human-like features related to precision grasping.

Conclusions: These results reinforce previous hypotheses relating the origin of refined manipulation of natural objects--not stone tool-making--with the relaxation of locomotor selection pressures on the forelimbs. This suggests that human hand length proportions are largely plesiomorphic, in the sense that they more closely resemble the relatively short-handed Miocene apes than the elongated hand pattern of extant hominoids. With the advent of terrestrial bipedalism, these hand proportions may have been co-opted by early hominins for enhanced manipulative capabilities that, in turn, would have been later co-opted for stone tool-making in the genus Homo, more encephalized than the previous australopiths. This hypothesis remains may be further tested by the finding of more complete hands of unequivocally biped early hominins.

Figure 1. Modern human thumb and index finger (right hand) during pad-to-pad precision grasping in ulnar view.

The box shows the anatomy of the pollical distal phalanx and its relationship with soft structures related to refined manipulation: a huge proximopalmar fossa (orange), associated with a palmarly protruding ridge (red) for insertion of the flexor pollicis longus; a compartmentalized digital pulp to accommodate the shape of the object being manipulated; this is reflected in the presence of an ungual fossa (green), associated to the large and mobile proximal pulp, as well as a wide apical tuberosity associated with the smaller and less mobile distal pulp; and finally, the ungual spines (yellow), where the collateral intraosseous ligaments that sustain the nail bed insert.

Figure 2. Morphological comparisons of pollical distal phalanges in African apes, extant humans and selected hominins.

Specimens are showed in palmar (top), oblique proximopalmar (middle) and lateral (bottom) views, and scaled to the same length to easily visualize the morphological differences. The main features related to human-like precision grasping are indicated in the middle row (same colors as in Figure 1), whereas the palmarly protruding insertion for the flexor pollicis longus has been further signaled in lateral view (red arrows in the lower row). Note that, although with several morphological differences, all the features related to refined manipulation in modern humans are already present in the late Miocene Orrorin. By the way, the OH 7 specimen, besides its odd overall proportions, neither shows a distinctive insertion for the flexor muscle, nor a compartmentalized digital pulp. All the phalanges belong to a right thumb. Scale bars represent 5 mm.

Figure 3. Principal components analysis (PCA) based on six shape variables of the pollical distal phalanx.

Blue, Papio; red, Pongo; yellow, H. sapiens; green, Gorilla; grey, Pan. The PC 1 largely reflects the proportions of the tuft and shaft, while the PC 2 is more related to the proportions of the base. The Orrorin PDP overlaps with modern humans in both principal components, and later hominins also resemble modern humans in both components—although to a lesser degree. Paranthropus robustus and OH 7 constitute an exception, because they fall within the human range across the PC 2, but depart from the remaining taxa on the PC 1 by showing exceptionally wide PDPs (Figures 2 and 3). See text for further explanation. Figures at the corners represent the outline of these phalanges in palmar and lateral views.

Figure 4. Boxplots of distal phalangeal robusticity in selected extant taxa, Neandertals, OH 7 and Paranthropus robustus.

Robusticity refers to apical tuft width (a) in relation to maximum length (b) of the distal pollical and middle finger phalanges (left and right, respectively; see Materials and for further details). Horizontal lines represent the median values, whereas the boxes represent the 25% and 75% percentiles, the whiskers the maximum-minimum ranges and circles are outliers. OH 7, like Paranthropus robustus, display a robusticity pattern convergent with quadrupedal monkeys (Macaca and Papio), in which the pollical distal phalanx is disproportionally robust relative to that from the middle finger. Note that the pollical and nonpollical distal phalanges attributed to P. robustus may not belong to the same individual.