Changing While Staying the Same: Preservation of Structural Continuity During Limb Evolution by Developmental Integration

Abstract

More than 150 years since Charles Darwin published "On the Origin of Species", gradual evolution by natural selection is still not fully reconciled with the apparent sudden appearance of complex structures, such as the bat wing, with highly derived functions. This is in part because developmental genetics has not yet identified the number and types of mutations that accumulated to drive complex morphological evolution. Here, we consider the experimental manipulations in laboratory model systems that suggest tissue interdependence and mechanical responsiveness during limb development conceptually reduce the genetic complexity required to reshape the structure as a whole. It is an exciting time in the field of evolutionary developmental biology as emerging technical approaches in a variety of non-traditional laboratory species are on the verge of filling the gaps between theory and evidence to resolve this sesquicentennial debate.

Fig. 1

Tissue origins of the musculoskeletal system. Lateral plate mesoderm cells in the presumptive limb region delaminate and give rise to limb bud mesenchymal cells. The lateral plate-derived mesenchymal cells will ultimately produce muscle connective tissues, tendons, skeleton, and ligaments in the limb. In contrast, limb muscles originate from precursor cells that delaminate from ventral–lateral somite and migrate into limb bud.

Fig. 2

Tissue interactions and accommodation in limb musculoskeltal development. Dorsal and ventral muscle masses in the limb bud are segregated and shaped into individual muscle groups by the lateral plate-derived connective tissues, especially muscle connective tissues. Once muscle, tendon, and skeleton are connected, mechanical forces from muscle contraction (arrows on muscle) stimulate bone shape modifications including joint morphogenesis, longitudinal and circumferential growth, curvature, and enthesis formation. If the evolutionary change in limb morphologies affects locomotor activity, the behavioral change will alter mechanical loading on bones and further reshape skeletal morphologies.