A median fin derived from the lateral plate mesoderm and the origin of paired fins

Creators: Tzung, Keh-Weei; Lalonde, Robert L.; Prummel, Karin D.; Mahabaleshwar, Harsha; Moran, Hannah R.; Stundl, Jan; Cass, Amanda N.; Le, Yao; Lea, Robert; Dorey, Karel; Tomecka, Monika J.; Zhang, Changqing; Brombacher, Eline C.; White, William T.; Roehl, Henry H.; Tulenko, Frank J.; Winkler, Christoph; Currie, Peter D.; Amaya, Enrique; Davis, Marcus C.; Bronner, Marianne E.¹; Mosimann, Christian; Carney, Tom J.

1. California Institute of Technology

Abstract

The development of paired appendages was a key innovation during evolution and facilitated the aquatic to terrestrial transition of vertebrates. Largely derived from the lateral plate mesoderm (LPM), one hypothesis for the evolution of paired fins invokes derivation from unpaired median fins via a pair of lateral fin folds located between pectoral and pelvic fin territories¹. Whilst unpaired and paired fins exhibit similar structural and molecular characteristics, no definitive evidence exists for paired lateral fin folds in larvae or adults of any extant or extinct species. As unpaired fin core components are regarded as exclusively derived from paraxial mesoderm, any transition presumes both co-option of a fin developmental programme to the LPM and bilateral duplication². Here, we identify that the larval zebrafish unpaired pre-anal fin fold (PAFF) is derived from the LPM and thus may represent a developmental intermediate between median and paired fins. We trace the contribution of LPM to the PAFF in both cyclostomes and gnathostomes, supporting the notion that this is an ancient trait of vertebrates. Finally, we observe that the PAFF can be bifurcated by increasing bone morphogenetic protein signalling, generating LPM-derived paired fin folds. Our work provides evidence that lateral fin folds may have existed as embryonic anlage for elaboration to paired fins.

Copyright and License

© The Author(s) 2023. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Acknowledgement

We thank K. Poss and M. Tanaka for providing zebrafish and medaka hand2 plasmids, respectively; Z. Gong for the transgenic fish line TgBAC(hand2:EGFP); D. Traver for input on the first iteration of Dendra2 transgenics; Y.-K. Tea for input; and K. P. Lim of the Lee Kong Chian Natural History Museum, Singapore for assisting with the frilled shark specimen. We also thank the Nanyang Technological University Zebrafish facility, the NTU Optical Bio-Imaging Centre (NOBIC), Colorado University (CU) Anschutz zebrafish care staff and all past and present members of our teams for continued support. This work was funded by the Industry Aligned Fund (IAF) Agency for Science, Technology and Research (grant to T.J.C. and K.-W.T.); Ministry of Education (MoE) Tier 3 (grant 2016-T3-1-005 to T.J.C., C.W. and H.M.); Ministry of Education (MoE) Tier 1 (grant 2016-T1-001-055 to T.J.C. and C.Z.); Ministry of Education (MoE) Tier 2 (grant MOE-T2EP30221-0008 to C.W.); the Company of Biologists (travelling fellowship to M.J.T.); the National Science Foundation (grants IOS-1853949 to M.C.D. and 2203311 to C.M.); the Swiss National Science Foundation Sinergia (grant CRSII5_180345 to C.M.); the Swiss Bridge Foundation (C.M.); Additional Ventures Single Ventricle Research Fund (SVRF) (grant 1048003 to C.M.); the University of Colorado School of Medicine Anschutz Medical Campus and the Children’s Hospital Colorado Foundation (C.M.); the National Institutes of Health (NIH), National Institute of General Medical Sciences (grants 1T32GM141742-01 to H.R.M. and 3T32GM121742-02S1 to H.R.M.); Australian Research Council (discovery grant DP200103219 to F.J.T. and P.D.C); National Health and Medical Research Council (senior principal research fellow APP1136567 to P.D.C.); and the NIH (grant R35NS111564 to J.S. and M.E.B.). Jan Stundl is supported by funding from the European Union’s Horizon 2020 research and innovation program under Marie Sklodowska-Curie grant agreement No. 897949.

Contributions

Experiments were conceived and designed by T.J.C., C.M., K.-W.T., M.E.B., M.C.D., E.A., P.D.C., C.W. and H.H.R. and were performed and analysed by K.-W.T., R.L.L., K.D.P., J.S., H.M., H.R.M., A.N.C., Y.L., R.L., K.D., M.J.T., C.Z., E.C.B., W.T.W. and F.J.T. The manuscript was written by K.-W.T. and T.J.C., with editing and input from C.M., J.S., A.N.C., M.C.D., F.J.T., P.D.C., R.L.L., K.D.P. and E.A.

Data Availability

The authors confirm that all relevant data are provided in this paper and in its Extended Data files. The data for measurements of fin size and cell number in Extended Data Fig. 3m–o are available in Figshare with the identifier https://doi.org/10.6084/m9.figshare.22269769. Source data are provided with this paper.

Conflict of Interest

The authors declare no competing interests.

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