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

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, Marina Marcet-Houben, Dina Navon, Ali Andrescavage, Ksenia Skvortsova, Paul Edward Duckett, Álvaro González-Rajal, Ozren Bogdanovic, Johan H. Gibcus, Liyan Yang, Lourdes Gallardo-Fuentes, Ismael Sospedra, Javier Lopez-Rios, Fabrice Darbellay, Axel Visel, Job Dekker, Neil Shubin, Toni Gabaldón, Tetsuya Nakamura (), Juan J. Tena (), Darío G. Lupiáñez (), Daniel S. Rokhsar () and José Luis Gómez-Skarmeta
Additional contact information
Ferdinand Marlétaz: University College London
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
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
Christine Hirschberger: University of Cambridge
Marina Marcet-Houben: Barcelona Supercomputing Centre (BCS-CNS)
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
Paul Edward Duckett: Garvan Institute of Medical Research
Álvaro González-Rajal: Garvan Institute of Medical Research
Ozren Bogdanovic: Garvan Institute of Medical Research
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
Axel Visel: Lawrence Berkeley National Laboratory
Job Dekker: University of Massachusetts Chan Medical School
Neil Shubin: University of Chicago
Toni Gabaldón: Barcelona Supercomputing Centre (BCS-CNS)
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
José Luis Gómez-Skarmeta: Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía

Nature, 2023, vol. 616, issue 7957, 495-503

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41586-023-05868-1

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