Molecular mechanisms underlying the exceptional adaptations of batoid fins

Tetsuya Nakamura; Jeff Klomp; Joyce Pieretti; Igor Schneider; Andrew R. Gehrke; Neil H. Shubin

doi:10.1073/pnas.1521818112

Contributed by Neil H. Shubin, November 5, 2015 (sent for review September 18, 2015; reviewed by Karen D. Crow and Clifford J. Tabin)

Significance

With 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.

Abstract

Extreme 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.

Footnotes

↵¹To whom correspondence should be addressed. Email: nshubin{at}uchicago.edu.

Author contributions: T.N. and J.P. designed research; T.N. and J.P. performed research; T.N., J.K., J.P., I.S., A.R.G., and N.H.S. analyzed data; and T.N., J.K., J.P., I.S., A.R.G., and N.H.S. wrote the paper.
Reviewers: K.D.C., San Francisco State University; and C.J.T., Harvard Medical School.
The authors declare no conflict of interest.
Data deposition: The sequences reported in this paper (S. rotifer Hoxa5 and C. plagiosum Gli3) have been deposited in the GenBank database (accession nos. KT425371 and KT425372). Transcriptome sequencing data have been deposited at the National Center for Biotechnology Information Sequence Read Archives (NCBI SRA), www.ncbi.nlm.nih.gov/sra (BioProject accession code PRJNA288370).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1521818112/-/DCSupplemental.

Freely available online through the PNAS open access option.