The evolution of human and ape hand proportions

Abstract

Human hands are distinguished from apes by possessing longer thumbs relative to fingers. However, this simple ape-human dichotomy fails to provide an adequate framework for testing competing hypotheses of human evolution and for reconstructing the morphology of the last common ancestor (LCA) of humans and chimpanzees. We inspect human and ape hand-length proportions using phylogenetically informed morphometric analyses and test alternative models of evolution along the anthropoid tree of life, including fossils like the plesiomorphic ape Proconsul heseloni and the hominins Ardipithecus ramidus and Australopithecus sediba. Our results reveal high levels of hand disparity among modern hominoids, which are explained by different evolutionary processes: autapomorphic evolution in hylobatids (extreme digital and thumb elongation), convergent adaptation between chimpanzees and orangutans (digital elongation) and comparatively little change in gorillas and hominins. The human (and australopith) high thumb-to-digits ratio required little change since the LCA, and was acquired convergently with other highly dexterous anthropoids.

Figure 1. Intrinsic hand proportions of humans and other anthropoid primates.

(a) Drawings of a chimpanzee and human hands are shown to similar scale. (b) Relative length of the thumb=pollical/fourth ray lengths (minus distal fourth phalanx; see inset). Box represents the interquartile range, centerline is the median, whiskers represent non-outlier range and dots are outliers. The ranges of humans and modern apes are highlighted (green and red-shaded areas, respectively). Samples for each boxplot are Homo sapiens (n=40), Pan troglodytes (n=34), Pan paniscus (n=12), Gorilla beringei (n=21), Gorilla gorilla (n=13), Pongo abelii (n=8), Pongo pygmaeus (n=19), Hylobatidae (n=14), Theropithecus (n=5), Papio (n=50), Mandrillus (n=3), Macaca (n=18), Nasalis (n=14), Cebus (n=11) and Alouatta (n=8). The values for Pr. heseloni and Ar. ramidus are projected onto the remaining taxa to facilitate visual comparisons.

Figure 2. Extrinsic hand proportions of humans and other anthropoid primates.

(a) Principal components analysis of the body mass-adjusted hand lengths. (b) Summary of the contribution of each hand element in selected anthropoids. Species are arranged by maximum length of ray IV (notice that the thumb does not follow the same trend). ARA-VP-6/500 L refers to an iteration of Ar. ramidus with an estimated body mass of 50.8 kg, whereas ARA-VP-6/500 S uses a smaller estimate of 35.7 kg.

Figure 3. Time-calibrated phylogenetic tree showing the estimated adaptive regimes in our anthropoid sample.

Adaptive optima are based on the two major axes of extrinsic hand proportions (EHP) variation between extant and fossil species (accounting for 94.5% of the variation). Branches are colour-coded according to different adaptive regimes (revealing that Pan and Pongo -red edges- are convergent). Clades are colour-coded (circles) as follows: brown, platyrrhines; dark green, cercopithecids; purple, hylobatids; light green, orangutans; red, gorillas; orange, chimpanzees; pink, fossil hominins; light blue, modern humans. The nodes corresponding to the last common ancestor (LCA) of great apes-humans and chimpanzees-humans are highlighted.

Figure 4. The evolutionary history of human and ape hand proportions.

Phylomorphospace projection of the phylogeny presented in Fig. 3 onto the two first principal components (PCs) of extrinsic hand proportions (EHP) in extant and fossil species. Taxa are colour-coded as in the phylogenetic tree; internal nodes (that is, ancestral-states reconstructed using maximum likelihood) are also indicated, highlighting the positions in shape space of the great ape-human and chimpanzee-human LCAs (plus 95% confidence intervals for the latter estimate). (a) EHP of Ardipithecus ramidus estimated using 50.8 kg. Owing to space constrictions, macaque species are not labelled. (b) Iteration using 35.7 kg for Ar. ramidus. Outlines (scaled to similar length) of extant and fossil apes and Ar. ramidus are plotted in this phylomorphospace to help visualizing major shape changes occurred during ape and human hand evolution. Panels (c) and (d) depict the EHP of chimpanzees and humans vis-à-vis their reconstructed last common ancestor (LCA) assuming, respectively, 50.8 kg and 35.7 kg for Ar. ramidus.

Figure 5. The hand of the late Miocene ape Hispanopithecus laietanus.

Its reconstructed hand is displayed in dorsal (a) and palmar (b) views, and together with its associated skeleton (c). This species represents the earliest specialized adaptations for below-branch suspension in the fossil ape record, although its hand combining short metacarpals and long phalanges, dorsally oriented hamato-metacarpal and metacarpo-phalangeal joints, presents no modern analogues. The phylogenetic position of Hispanopithecus is still highly debated: stem great ape (d), stem pongine (e) or stem hominine (e)? Scale bars represent 10 cm. Reconstruction of the IPS 18800 (Hispanopithecus) skeleton in panel (c) reproduced with the permission of Salvador Moyà-Solà and Meike Köhler.

Figure 6. Reconstructed evolutionary histories of human and ape digital extrinsic proportions.

The phylomorphospace approach was limited to the three long bones of ray IV to include the fossil ape Hispanopithecus laietanus and Ateles species. The same analysis was iterated with the large (a) and small (b) body mass estimates of Ardipithecus ramidus (finding no differences in the overall evolutionary pattern). Internal nodes (that is, ancestral-state reconstructions) and branch lengths are indicated for three different phylogenetic hypotheses: Hi. laietanus as a stem great ape (black), a stem pongine (orange) and stem African ape (red). Species names are indicated in (a) with the exception of macaques.