The evolutionary origin of digit patterning

Abstract

The evolution of tetrapod limbs from paired fins has long been of interest to both evolutionary and developmental biologists. Several recent investigative tracks have converged to restructure hypotheses in this area. First, there is now general agreement that the limb skeleton is patterned by one or more Turing-type reaction-diffusion, or reaction-diffusion-adhesion, mechanism that involves the dynamical breaking of spatial symmetry. Second, experimental studies in finned vertebrates, such as catshark and zebrafish, have disclosed unexpected correspondence between the development of digits and the development of both the endoskeleton and the dermal skeleton of fins. Finally, detailed mathematical models in conjunction with analyses of the evolution of putative Turing system components have permitted formulation of scenarios for the stepwise evolutionary origin of patterning networks in the tetrapod limb. The confluence of experimental and biological physics approaches in conjunction with deepening understanding of the developmental genetics of paired fins and limbs has moved the field closer to understanding the fin-to-limb transition. We indicate challenges posed by still unresolved issues of novelty, homology, and the relation between cell differentiation and pattern formation.

Keywords: Development; Fin; Genetics; Novelty; Self-organization; Turing.

Fig. 1

Fin-to-limb transition involved a suite of anatomical changes including loss of dermal fin rays and the acquisition of digits. a Pectoral fin skeleton of Tiktaalik roseae, an elpistostegid fish. The fin contains both dermal skeleton (lepidotrichia) and endochondral skeleton. Illustration modified from Shubin et al. [64]. b Forelimb skeleton of Acanthostega gunnari, a stem tetrapod. The limb exhibits a polydactylous pattern, which is characteristic of the earliest limbs. Illustration modified from Coates et al. [65] follows that labeling scheme, although other labeling schemes have been proposed for autopodial elements (e.g., [66]). c Forelimb skeleton of human (Homo sapiens). This limb shows a pentadactyl pattern and also mesopodial (wrist) elements; these features characterize the crown-group tetrapod condition. Illustration modified from Owen [67]. For each illustration, anterior is oriented to the left. Extinct taxa are noted with a dagger (†)

Fig. 2

Experimental manipulation of Gal8 affects zeugopod, stylopod, and autopod development in the avian wing. Left—wing bud from a 5-day chicken embryo injected with Gal8 protein, grown for a day and then isolated, fixed, and stained for cartilage with Alcian blue. Right—the control, contralateral wing bud (reflected). Experimental treatment results in complete absence of chondrified primordia in the autopod, dysmorphic, aberrantly arranged primordia in the zeugopod, and a weakly stained, poorly developed stylopod. The control limb shows well-developed and stained cartilage primordia in the stylo-, zeugo-, and autopodial regions. Images adapted from [40]