Molecular mechanisms underlying the exceptional adaptations of batoid fins

Contributed by Neil H. Shubin, November 5, 2015 (sent for review September 18, 2015; reviewed by Karen D. Crow and Clifford J. Tabin)
December 7, 2015
112 (52) 15940-15945

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.

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Data Availability

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).

Acknowledgments

We thank Jonathan D. Gitlin, Andrew Latimer, Rebecca Thomason, David Remsen, Scott H. Bennett, and the Marine Resource Center of The Marine Biological Laboratory for the experimental space and husbandry of skate and sharks; Benjamin L. King (Mount Desert Island Laboratory) for sharing unpublished skate transcriptome information; Glen Randall and Ana Shulla (University of Chicago) for the cell culture space; John Westlund (University of Chicago) for the elegant illustrations in this paper; and Michael Coates, Justin Lemberg, Noritaka Adachi, and Darcy Ross (University of Chicago) for stimulating discussion. This work was supported by The Brinson Foundation and the University of Chicago Biological Sciences Division (to N.H.S.); a Japanese Society for the Promotion of Science (JSPS) Postdoctoral Fellowship for Research Abroad, Uehara Memorial Foundation Research Fellowship, and Marine Biological Laboratory Research Grant (to T.N.); National Science Foundation Grant IOS-1355057 (to J.K.); Graduate Assistance in Areas of National Need Grant P200A120178 (to J.P.); NIH Grant T32 HD055164 and National Science Foundation Doctoral Dissertation Improvement Grant 1311436 (to A.R.G.); Brazilian National Council for Scientific and Technological Development Grants 402754/2012-3 and 477658/2012-1 (to I.S.); and Institutional Development Awards of NIH P20GM103423 and P20GM104318.

Supporting Information

Appendix (PDF)
Supporting Information

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 112 | No. 52
December 29, 2015
PubMed: 26644578

Classifications

Data Availability

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).

Submission history

Published online: December 7, 2015
Published in issue: December 29, 2015

Keywords

  1. skate
  2. fin
  3. evolution
  4. development
  5. AER

Acknowledgments

We thank Jonathan D. Gitlin, Andrew Latimer, Rebecca Thomason, David Remsen, Scott H. Bennett, and the Marine Resource Center of The Marine Biological Laboratory for the experimental space and husbandry of skate and sharks; Benjamin L. King (Mount Desert Island Laboratory) for sharing unpublished skate transcriptome information; Glen Randall and Ana Shulla (University of Chicago) for the cell culture space; John Westlund (University of Chicago) for the elegant illustrations in this paper; and Michael Coates, Justin Lemberg, Noritaka Adachi, and Darcy Ross (University of Chicago) for stimulating discussion. This work was supported by The Brinson Foundation and the University of Chicago Biological Sciences Division (to N.H.S.); a Japanese Society for the Promotion of Science (JSPS) Postdoctoral Fellowship for Research Abroad, Uehara Memorial Foundation Research Fellowship, and Marine Biological Laboratory Research Grant (to T.N.); National Science Foundation Grant IOS-1355057 (to J.K.); Graduate Assistance in Areas of National Need Grant P200A120178 (to J.P.); NIH Grant T32 HD055164 and National Science Foundation Doctoral Dissertation Improvement Grant 1311436 (to A.R.G.); Brazilian National Council for Scientific and Technological Development Grants 402754/2012-3 and 477658/2012-1 (to I.S.); and Institutional Development Awards of NIH P20GM103423 and P20GM104318.

Authors

Affiliations

Tetsuya Nakamura
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
Jeff Klomp
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
Joyce Pieretti
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
Igor Schneider
Instituto de Ciencias Biologicas, Universidade Federal do Para, 66075 Belem, Brazil
Andrew R. Gehrke
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
Neil H. Shubin1 [email protected]
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
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.

Competing Interests

The authors declare no conflict of interest.

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    Molecular mechanisms underlying the exceptional adaptations of batoid fins
    Proceedings of the National Academy of Sciences
    • Vol. 112
    • No. 52
    • pp. 15767-E7307

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