A shift in anterior-posterior positional information underlies the fin-to-limb evolution.

Koh Onimaru,Susumu Hyodo,Shigehiro Kuraku,Mikiko Tanaka,Wataru Takagi,James Sharpe

doi:10.7554/elife.07048

Abstract

The pectoral fins of ancestral fishes had multiple proximal elements connected to their pectoral girdles. During the fin-to-limb transition, anterior proximal elements were lost and only the most posterior one remained as the humerus. Thus, we hypothesised that an evolutionary alteration occurred in the anterior-posterior (AP) patterning system of limb buds. In this study, we examined the pectoral fin development of catshark (Scyliorhinus canicula) and revealed that the AP positional values in fin buds are shifted more posteriorly than mouse limb buds. Furthermore, examination of Gli3 function and regulation shows that catshark fins lack a specific AP patterning mechanism, which restricts its expression to an anterior domain in tetrapods. Finally, experimental perturbation of AP patterning in catshark fin buds results in an expansion of posterior values and loss of anterior skeletal elements. Together, these results suggest that a key genetic event of the fin-to-limb transformation was alteration of the AP patterning network.

Highlights

Regulatory interactions between transcriptional factors play important roles for interpreting a morphogen gradient as positional information (Balaskas et al, 2012)
The fin-to-limb transformation is a prominent but still unsolved example of morphological evolution. 150 years ago Carl Gegenbaur subdivided the skeletal elements of shark pectoral fins into three segments along the anterior–posterior (AP) axis: propterygium, mesopterygium, and metapterygium (Gegenbaur, 1865) (Figure 1A), which are found in the majority of chondrichthyans, none-teleost actinopterygians, placoderms, and acanthodians (Orvig, 1962; Coates, 1994, 2003)
To investigate changes in AP patterning during the fin-to-limb transition, we first cloned a number of AP patterning genes from the non-model species Scyliorhinus canicula (Figure 1B–H and Figure 1—figure supplement 1 for phylogentic analyses)

Summary

Introduction

Regulatory interactions between transcriptional factors play important roles for interpreting a morphogen gradient as positional information (Balaskas et al, 2012). Onimaru et al show that the pattern of gene expression in the catshark fin bud is different to that of the mouse limb bud. In stage 30 S. canicula embryos (staged according to Ballard et al, 1993), we found instead that the anterior genes Alx4, Pax9, Hand1, and Zic3 were expressed in broad domains, which extend more posteriorly than in the mouse (half the fin bud for Alx4, two-thirds for Pax9 and Hand1, and the whole axis for Zic3, Figure 1B–E).

Results

Conclusion