Function, ontogeny and canalization of shape variance in the primate scapula

Abstract

Primates have shoulders adapted to a wide range of locomotor functions from terrestrial pronograde quadrupedalism to highly arboreal suspensory behaviours. The shape of the scapula tightly follows these functional differences. Previous analyses of primate postcrania, including the scapula, indicate that quadrupedal monkeys are less variable than non-quadrupeds. It was previously suggested that this difference was due to a relationship between the strength of stabilizing selection and the functional demands of the upper limb. Here it is shown that intraspecific scapular shape variance is highly correlated with the degree of committed quadrupedalism. Primates that engage in frequent suspensory behaviours (e.g. apes and ateline monkeys) average twice the amount of shape variance as quadrupeds (e.g. Old World monkeys and Saimiri). Because this difference in intraspecific shape variance is apparent in infants and does not increase or decrease appreciably over ontogeny, it is not likely that differences in postnatal growth, neuromuscular control or environmental factors such as habitat structure/composition are the primary contributors to differences in adult shape variance. Instead variance in embryonic factors that affect the shape/size of the scapula or epigenetic factors associated with muscle attachments are more likely candidates. In particular, the heterogeneous functional demands of the non-quadrupedal shoulder probably reduce the stringency of stabilizing selection, resulting in the persistence into adulthood of increased amounts of embryonically generated scapular shape variance.

Fig. 1

The scapula of a typical committed terrestrial quadruped (top, macaque) and an arboreal suspensory non-quadruped (bottom, chimpanzee) in dorsal and ventral view. The side view of a generalized primate scapula is shown on the far right. The typical quadrupedal scapula is longer from vertebral border to glenoid and shorter from superior to inferior angles. In non-quadrupeds such as apes and ateline monkeys this pattern is largely reversed. Note the differences in the shape of the blade, and the orientation and size of the spine that discriminate the extremes of these two groups. Location of landmarks are shown on both specimens: (1) suprascapular notch; (2) superior angle; (3) point on the vertebral margin where the long axis of the scapular spine and the vertebral border meet; (4) inferior angle; (5) teres major fossa; (6) infraglenoid tubercle; (7) spinoglenoid notch; (8) medial extent of the trapezius attachment along the scapular spine; (9) inferior-most point on glenoid fossa; (10) greatest width of the glenoid fossa (lateral); (11) greatest width of the glenoid fossa (medial); (12) superior-most point on glenoid fossa; (13) shallowest point (maximal curvature) of the glenoid fossa; (14) coracoid prominence; (15) distal-most tip of the coracoid process (superior); (16) distal-most tip of the coracoid process (inferior); (17) distal-most point of the acromion.

Fig. 2

Three-dimensional scatterplots of Procrustes-aligned landmark data for adult Macaca fasicularis (left, blue) and Pan troglodytes (right, red). Macaques exhibit significantly less shape variance at this ontogenetic stage (V = 0.0034) and earlier stages as compared with chimpanzees (V = 0.0072) (t = 6.221, P = 0.000).

Fig. 3

Bivariate plot illustrating the relationship of locomotor function (QI) with shape variance in: (a) infants (r² = 0.933, d.f. = 5, P = 0.000), (b) juveniles (r² = 0.683, d.f. = 9, P = 0.002), and (c) adults (r² = 0.815, d.f. = 15, P = 0.000). Dashed lines represent regressions through the data.

Fig. 4

Boxplot showing the distribution of shape variance when species are combined into two groups comprised of non-quadrupeds (QI < 0.25: Ateles, Hylobates, Gorilla, Lagothrix, Pan paniscus, Pan troglodytes, Pongo and Symphalangus) and quadrupeds (QI > 0.50: Alouatta, Cercocebus, Cercopithecus, Colobus, Macaca, Nasalis, Papio, Presbytis and Saimiri) for three ontogenetic stages (infant = m¹, juvenile = m², and adult = m³). All shape variances were calculated from Procrustes data standardized by centroid size to minimize overestimates due to ontogenetic size heterogeneity. Shape variance is higher in non-quadrupeds in all ontogenetic stages.

Fig. 5

Bivariate plot showing the relationship of the quadrupedalism index (QI) to the morphological integration index (EV, eigenvalue variance standardized by within-species shape variance) (r² = 0.464, d.f. = 14, P = 0.004). Dashed line represents a regression through the data.

Fig. 6

Boxplot comparing the distribution of the integration index (EV, eigenvalue variance standardized by within-species variance) in non-quadrupeds and quadrupeds. The mean EV of non-quadrupeds is significantly lower than that of quadrupeds (1000 resampled replicates, P = 0.000).

Fig. 7

Bar graph showing ontogenetic trends in shape variance for the species in which data are available for all stages (blue: infant; red: juvenile; yellow: adult).