Did our ancestors knuckle-walk?

Richmond and Strait reply

Dainton's argument that knuckle-walking may have evolved in parallel in Gorilla and the Pan/Homo ancestor is possible, but unparsimonious. Moreover, patterns of African-ape carpal growth¹ do not provide an adequate test of knuckle-walking homology, given evidence that development does not always faithfully reflect homology². Siamangs and gibbons differ in skeletal growth³, but no one disputes the homology of their suspensory specializations.

Regarding Dainton's points about our functional interpretation, an obtuse angulation between the scaphoid and lunate facets resists compressive stresses as part of a complex that stabilizes the wrist in extension during knuckle-walking⁴. With respect to the statistics, our cluster analysis (Fig. 2c), the Mahalanobis D² distances, and posterior probabilities of group assignment show that A. afarensis and A. anamensis radii are more similar to Gorilla and Pan than either are to Pongo. Finally, although knuckle-walking traits may have arisen to serve extension-limiting functions in other forms of locomotion, there is no evidence to support this. Our hypothesis meets Lauder's definition of a “best-case scenario”⁵, in which the extinct taxon whose behaviour is being reconstructed lies within a clade that includes extant members for which a form is exclusively related to a function.

Lovejoy et al. misinterpret our discussion of radio-scaphoid joint function. All the anthropoids we examined have scaphoid notches. However, the morphology of the notch, in combination with features such as distal projection, distinguishes knuckle-walkers from other taxa (see http://www.anthro.uiuc.edu/faculty/richmond/hominidradii.html). African apes differ from other anthropoids in that the radius and scaphoid conform posteriorly after minimal extension, such that “no further movement is possible without disengaging the articular surfaces . . . this part of the joint achieves a 'locked' or 'close-packed' position”⁴. Such terminology is conventional⁶. Muscle and other tissues can play a role in promoting joint stability, and we explicitly cited experimental evidence on the subject. However, the digital flexors are not recruited during knuckle-walking at slow-to-moderate speeds. Active recruitment is crucial in maintaining tension to enable the tendons to store and return elastic energy⁷. Moreover, passive tension of the digital flexors is unlikely to be significant during knuckle-walking because the fingers are flexed. Regardless, active or passive muscle tension across the wrist does not necessarily diminish the importance of joint morphology in providing stability.

Lovejoy et al. suggest developmental hypotheses to explain variation in joint morphology. We disagree with their implication that species-specific aspects of joint shape have little hereditary basis. During early development, joint morphology is heavily influenced by genetic factors, to the extent that normal articular topography will appear even if the adjacent surface is absent or if limb paralysis is induced⁸. Although the employment of abnormal positional behaviours influences articular development⁹, it is unclear how, or whether, the absence of specific behaviours influences joint growth. Current evidence suggests that bone length and aspects of joint shape are not heavily influenced by physiological variations in activity during growth, unlike trabecular structure, and cortical bone thickness, density and curvature¹⁰. Thus, functionally sensitive features such as femoral bicondylar angle and phalangeal curvature suggest both bipedalism and arboreality in Australopithecus, whereas radiocarpal joint shape might be a product of evolutionary history.

Although Lovejoy et al. reject the possibility that functionally relevant traits might be retained through phylogenetic inertia, they have argued¹¹, in reference to australopithecine joint morphology, that one cannot “expect an animal that has recently evolved bipedality to no longer have any anatomical characters that are not also found in modern-day apes”. This thesis is central to their^11,12 long-held argument that early australopithecines are obligate bipeds but retain arboreal features without practising arboreality. It might be concluded from Lovejoy et al.'s present developmental argument that these very same fossil hominids are knuckle-walkers. We doubt they believe this, and neither do we. Phylogenetic inertia remains the most plausible interpretation of the morphology we identified. How functionally to interpret primitive retentions is the central problem in reconstructing behaviour in fossil hominids. We still do not fully understand the genetic and epigenetic influences on bone development, and need to identify bone morphology that provides a faithful record of an individual's biomechanical activity.