Canalization, developmental stability, and morphological integration in primate limbs

Abstract

Canalization and developmental stability refer to the tendency of developmental processes to follow particular trajectories, despite external or internal perturbation. Canalization is the tendency for development of a specific genotype to follow the same trajectory under different conditions (different environments or different genetic backgrounds), while developmental stability is the tendency for the development of a specific genotype to follow the same trajectory under the same conditions. Morphological integration refers to the tendency for structures to show correlated variation because they develop in response to shared developmental processes or function in concert with other structures. All three phenomena are emergent properties of developmental systems that can affect the interaction of development and evolution. In this paper, we review the topics of canalization, developmental stability, and morphological integration and their relevance to primate and human evolution. We then test three developmentally motivated hypotheses about the patterning of variability components in the mammalian limb. We find that environmental variances and fluctuating asymmetries (FA) increase distally along the limb in adult macaques but not in fetal mice. We infer that the greater variability of more distal segments in macaques is due to postnatal mechanical effects. We also find that heritability and FA are significantly correlated when different limb measurements are compared in fetal mice. This supports the idea that the mechanisms underlying canalization and developmental stability are related. Finally, we report that the covariation structure of fore-and hindlimb skeletal elements shows evidence for morphological integration between serially homologous structures between the limbs. This is evidence for the existence of developmental modules that link structures between the limbs. Such modules would produce covariation that would need to be overcome by selection for divergence in hind-and forelimb morphology. Yrbk Phys Anthropol 45: 131-158, 2002.

Limb bone bilateral asymmetry: variability and commonality among modern humans

“…We found no significant correlations within individuals between asymmetry in bone lengths and asymmetry in diaphyseal breadths, supporting their relative independence. This suggests that lengths and diaphyseal breadths are ''modular'' in the sense of independent development, or perhaps simply that developmental integration of limb lengths and breadths is overridden to different extents by subsequent, stronger environmental effects on breadths (for a general discussion, see Hallgrímsson et al, 2002). It may be that, although limbs are potentially subject to the same perturbations during development, differing degrees of canalization (Hallgrímsson et al, 2002(Hallgrímsson et al, , 2003 may leave some bone dimensions more sensitive to these effects both in utero and after birth.…”

“…Of course, forearm loading is also shared between the radius and ulna, but any variation in ulnar bilateral asymmetry (not measured in this study) apparently does not negate asymmetry correlations between the humerus and radius. The ipsilateral correlations of asymmetry in bone length in both the upper and lower limbs may relate to developmental mechanisms of control over bone length within limbs, although experimental support for this is equivocal (Hallgrímsson et al, 2002). Further investigations of modularity and morphological integration during development may elucidate the covariation of bilateral asymmetry between different types of traits and regions of the limbs and the interaction between genetic and environmental (particularly mechanical) influences on these associations.…”

Gracility of the modernHomo sapiensskeleton is the result of decreased biomechanical loading

“…Alternatively, it has been suggested that the low bone-volume fraction observed in human thoracic vertebrae and the first and second metatarsals are the result of systemic physiological differences between humans and apes (14,16). These studies do not suggest the mechanism or the function of this systemic gracility, but one potential explanation may be selection for increased tissue economy in hominins (5,(33)(34)(35).…”

The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

“…Nonetheless, quantitative approaches can estimate the developmental contribution to phenotypic integration in fossil taxa, even without identifying a specific developmental driver, by measuring fluctuating asymmetry (FA). Simply, whereas genetic and environmental perturbations affect symmetric traits similarly, developmental errors lead to random, nondirectional asymmetries in the morphology, thereby revealing patterns of direct developmental interactions among traits (22,(46)(47)(48)(49). By quantifying FA, one can test whether the patterns of direct developmental interactions correspond to major components of variation across individuals and among taxa, as would be expected if developmental integration is a significant constraint on evolutionary variation.…”