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The little skate genome and the evolutionary emergence of wing-like fins

Author

Listed:
  • Ferdinand Marlétaz

    (University College London
    Okinawa Institute of Science and Technology Graduate University)

  • Elisa de la Calle-Mustienes

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Rafael D. Acemel

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía
    Berlin Institute for Medical Systems Biology (BIMSB))

  • Christina Paliou

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Silvia Naranjo

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Pedro Manuel Martínez-García

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Ildefonso Cases

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Victoria A. Sleight

    (University of Cambridge
    University of Aberdeen)

  • Christine Hirschberger

    (University of Cambridge)

  • Marina Marcet-Houben

    (Barcelona Supercomputing Centre (BCS-CNS)
    Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology)

  • Dina Navon

    (Rutgers the State University of New Jersey)

  • Ali Andrescavage

    (Rutgers the State University of New Jersey)

  • Ksenia Skvortsova

    (Garvan Institute of Medical Research
    University of New South Wales)

  • Paul Edward Duckett

    (Garvan Institute of Medical Research)

  • Álvaro González-Rajal

    (Garvan Institute of Medical Research
    University of New South Wales)

  • Ozren Bogdanovic

    (Garvan Institute of Medical Research
    University of New South Wales)

  • Johan H. Gibcus

    (University of Massachusetts Chan Medical School)

  • Liyan Yang

    (University of Massachusetts Chan Medical School)

  • Lourdes Gallardo-Fuentes

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Ismael Sospedra

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Javier Lopez-Rios

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Fabrice Darbellay

    (Lawrence Berkeley National Laboratory
    University of Geneva)

  • Axel Visel

    (Lawrence Berkeley National Laboratory
    US Department of Energy Joint Genome Institute
    University of California)

  • Job Dekker

    (University of Massachusetts Chan Medical School
    Howard Hughes Medical Institute)

  • Neil Shubin

    (University of Chicago)

  • Toni Gabaldón

    (Barcelona Supercomputing Centre (BCS-CNS)
    Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology
    Catalan Institution for Research and Advanced Studies (ICREA)
    Instituto de Salud Carlos III)

  • Tetsuya Nakamura

    (Rutgers the State University of New Jersey)

  • Juan J. Tena

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

  • Darío G. Lupiáñez

    (Berlin Institute for Medical Systems Biology (BIMSB))

  • Daniel S. Rokhsar

    (Okinawa Institute of Science and Technology Graduate University
    University of California
    Chan-Zuckerberg Biohub)

  • José Luis Gómez-Skarmeta

    (Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía)

Abstract

Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments1,2. However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.

Suggested Citation

  • Ferdinand Marlétaz & Elisa de la Calle-Mustienes & Rafael D. Acemel & Christina Paliou & Silvia Naranjo & Pedro Manuel Martínez-García & Ildefonso Cases & Victoria A. Sleight & Christine Hirschberger , 2023. "The little skate genome and the evolutionary emergence of wing-like fins," Nature, Nature, vol. 616(7957), pages 495-503, April.
  • Handle: RePEc:nat:nature:v:616:y:2023:i:7957:d:10.1038_s41586-023-05868-1
    DOI: 10.1038/s41586-023-05868-1
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