Development and the evolvability of human limbs

Abstract

The long legs and short arms of humans are distinctive for a primate, the result of selection acting in opposite directions on each limb at different points in our evolutionary history. This mosaic pattern challenges our understanding of the relationship of development and evolvability because limbs are serially homologous and genetic correlations should act as a significant constraint on their independent evolution. Here we test a developmental model of limb covariation in anthropoid primates and demonstrate that both humans and apes exhibit significantly reduced integration between limbs when compared to quadrupedal monkeys. This result indicates that fossil hominins likely escaped constraints on independent limb variation via reductions to genetic pleiotropy in an ape-like last common ancestor (LCA). This critical change in integration among hominoids, which is reflected in macroevolutionary differences in the disparity between limb lengths, facilitated selection for modern human limb proportions and demonstrates how development helps shape evolutionary change.

Fig. 1.

(A) The common genetic architecture of limbs, as demonstrated by their similar Hox patterning (gray, low expression; black, primary expression) (6), reflects their serial homology and suggests a hierarchical limb covariation structure apportioned between and within limbs (7, 8). Theoretical developmental and functional modules of the human limb are shown: stylopod (humerus and femur), zeugopod (radius/ulna, tibia/fibula), and autopod (hands, feet, and digits). (B) Covariation between developmental modules of the limbs in response to selection determines the phenotypic space (gray ellipses) and the independent evolvability of limbs. When correlations are low, phenotypic space is more evenly distributed (Upper Left). When correlations are high this space will tend toward individuals differing in size but with similar proportions (Bottom Right). The model predicts that the mosaic evolution of modern human limb proportions required reductions in integration. (C) Humans (black circle) have relative limb proportions that are distinct from apes (gray circles) and quadrupedal monkeys (white circles). The net direction of evolutionary change was an increase to relative leg length and a smaller decrease in relative arm length and is approximately orthogonal to interspecific allometry of quadrupedal relative limb proportions (dashed line). Data are based on ref. . (D) Selection in hominins occurred in at least two phases: (i) in early hominins such as the australopithecines [Au. afarensis (AL-288-1) and BOU-12/1, gray, reconstructed] relative leg length increased with smaller changes to relative arm length (18, 20, 55, 56) [note: estimated IMI of Ar. ramidus is comparable to Au. afarensis (25)], and (ii) in H. ergaster (KNM-WT15000) relative forearm length decreased and leg length further increased (18, 20, 21). This mosaic pattern indicates independent variation in the limbs and reduced integration. Locations of fossils are based on published descriptions and estimates (18, 20, 21, 55, 56).

Fig. 2.

(A) Anthropoid primates exhibit consistent developmental modularity of limbs. Within-limb modularity reflects varying functional signals (e.g., bipedalism in the hindlimb of humans and forelimb suspension in apes). Modules (partial correlations P < 0.05) are illustrated as boxes between elements. Modules are shaded relative to the strength of the estimated Fisher-z transformed correlation. Estimated Pearson correlation coefficient is shown. (MC, metacarpal; MT, metatarsal; R, radius; T, tibia; H, humerus; F, femur). Species arranged by phylogenetic relationship as shown at Bottom. (B) Humans are significantly less integrated compared to quadrupedal monkeys and similar to apes, indicating that reductions to integration and more independently evolvable limbs characterize both fossil hominins and hominoids. Box plots show the lower and upper quartile, median of resampled eigenvalue variance (VE) (10,000 replicates). Whiskers indicate the 95% confidence limit of the estimate. Dashed lines and shaded boxes show the average VE for hominoids (=1.79), cercopithecoids (=3.32), and ceboids (=2.90) and the 95% confidence interval, respectively.

Fig. 3.

Hominoid taxa have more variable interlimb proportions compared to cercopithecoid and ceboid monkeys as predicted by their reduced integration (all comparisons P < 0.05, Levene’s test). Each dot represents one species value. Black boxes show the mean of each group. (A) Comparison of relative arm and leg length for species with mixed function from each of the superfamilies (Table S11). (B) Comparison between suspensory apes to quadrupedal monkey species for the intermembral index (Table S12). (C) Comparison of primate radiations of comparable time depths and species numbers (Table S13).