A shift in anterior–posterior positional information underlies the fin-to-limb evolution
Koh Onimaru,
Shigehiro Kuraku,
Wataru Takagi,
Susumu Hyodo,
James Sharpe,
Mikiko Tanaka
Affiliations
Koh Onimaru
Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan; EMBL-CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain
Shigehiro Kuraku
Phyloinformatics Unit, RIKEN Center for Life Science Technologies, Kobe, Japan
Wataru Takagi
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan
Susumu Hyodo
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan
James Sharpe
EMBL-CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain
Mikiko Tanaka
Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan
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.
