Molecular mechanisms underlying the exceptional adaptations of batoid fins
Tuesday, 2016/01/05 | 08:13:57
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Tetsuya Nakamura, Jeff Klomp, Joyce Pieretti, Igor Schneider, Andrew R. Gehrke, and Neil H. Shubin EVOLUTION SignificanceWith pectoral fins that surround much of the body, by fusing to the head, the skate is a cartilaginous fish that has one of the most unique appendages of all vertebrates. Here, we use an unbiased RNA screen to uncover genetic pathways underlying this morphology. Unlike tetrapods and other fishes, skates induce a second growth center in the anterior region, by the redeployment of an ancient genetic module. We find that some of the genes involved in generating the anterior–posterior fin function differently in skates than they do in limbed animals. Our data reveal the mechanisms for the unique skate fin morphology and also provide insights into the genetic origins of fin variation and morphological innovation in paired appendages. AbstractExtreme novelties in the shape and size of paired fins are exemplified by extinct and extant cartilaginous and bony fishes. Pectoral fins of skates and rays, such as the little skate (Batoid, Leucoraja erinacea), show a strikingly unique morphology where the pectoral fin extends anteriorly to ultimately fuse with the head. This results in a morphology that essentially surrounds the body and is associated with the evolution of novel swimming mechanisms in the group. In an approach that extends from RNA sequencing to in situ hybridization to functional assays, we show that anterior and posterior portions of the pectoral fin have different genetic underpinnings: canonical genes of appendage development control posterior fin development via an apical ectodermal ridge (AER), whereas an alternative Homeobox (Hox)–Fibroblast growth factor (Fgf)–Wingless type MMTV integration site family (Wnt) genetic module in the anterior region creates an AER-like structure that drives anterior fin expansion. Finally, we show that GLI family zinc finger 3 (Gli3), which is an anterior repressor of tetrapod digits, is expressed in the posterior half of the pectoral fin of skate, shark, and zebrafish but in the anterior side of the pelvic fin. Taken together, these data point to both highly derived and deeply ancestral patterns of gene expression in skate pectoral fins, shedding light on the molecular mechanisms behind the evolution of novel fin morphologies.
See http://www.pnas.org/content/112/52/15940.abstract.html?etoc PNAS December 29 2015; vol. 112 no. 52: 15940–15945
Fig. 1. Appendage diversity and the skate unique fin. (A) The pectoral fin and forelimb skeleton in a variety of taxa. Chondrichthyan and basal actinopterygian fins are composed of three bones, pro-, meso-, and metapterygium, whereas the sarcopterygian appendage is a single rod of the metapterygium axis. The batoid fin is extremely wide along the A–P axis compared with other vertebrates. Dermal bones (derm) and endochondral bones (endo) are labeled by gray and black colors depending on the difference of its developmental mechanisms (36). (B–D) Alcian Blue-stained skeletal preparations of skate embryos at stages 30–32. mes, mesopterygium; met, metapterygium; pro, propterygium. Both pectoral and pelvic fins elongate along the A–P axis. (E) Immunostaining for phosphorylated histone H3 (green) and DAPI (blue) in the pectoral fin at stage 31. Image composed using tiled scanning by confocal microscope (Zeiss ZEN software). Inset, magnified portions of the anterior and central fin. Statistical analysis of cell proliferation rates in each portion can be found in SI Appendix, Fig. S1. (F and G) Summary of the developmental mechanisms of the tetrapod limb. At an early stage (F), Shh is expressed in the posterior limb bud, and 5′Hox genes show a gradient of expression. Fgf10 induces and maintains AER structure. In turn, Fgf8 and Wnt3 in AER stimulate cell proliferation in the limb mesenchyme. As the limb bud develops, 5′Hox genes mark the autopod domain, whereas 3′Hox genes are expressed in the proximal limb.
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