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Cited by 71Developmental Biology and Gene RegulationGenomics and Chromatin DynamicsChromosomal and Genetic Variations

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

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Marlétaz, Ferdinand, de la Calle-Mustienes, Elisa, Acemel, Rafael D., Paliou, Christina, Naranjo, Silvia, Martínez-García, Pedro Manuel, Cases, Ildefonso, Sleight, Victoria A. +23 more·2023·Nature
DOI 10.1038/s41586-023-05868-1PMC PMC10115646
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Abstract

Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments 1,2 . 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.

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  • A single inversion in the genome of skates and rays contributes to large fin sizes during development.

    “whereas a single inversion in the genome of skates and rays contributes to large fin sizes during development (154).”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [154]

    The ‘PCP pathway as a driver of fin expansion’ section links skate-specific genomic rearrangements to genes potentially involved in pectoral fin expansion, and reports reduced anterior fin expansion after PCP-pathway inhibition (page unavailable). It does not identify a single inversion as the contributor; the paper describes multiple rearrangements and candidate genes instead. (LLM, conf=0.88)

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Cited by

Sorted by citations

Authors
Marlétaz, F., de la Calle-Mustienes, E., Acemel, R. D., Paliou, C., Naranjo, S., Martínez-García, P. M., Cases, I., Sleight, V. A., Hirschberger, C., Marcet-Houben, M., Navon, D., Andrescavage, A., Skvortsova, K., Duckett, P. E., González-Rajal, Á., Bogdanovic, O., Gibcus, J. H., Yang, L., Gallardo-Fuentes, L., Sospedra, I., Lopez-Rios, J., Darbellay, F., Visel, A., Dekker, J., Shubin, N., Gabaldón, T., Nakamura, T., Tena, J. J., Lupiáñez, D. G., Rokhsar, D. S., & Gómez-Skarmeta, J. L.
Affiliations
  • Okinawa Institute of Science and Technology Graduate University (JP)
  • Consejo Superior de Investigaciones Científicas (ES)
  • University of Aberdeen (GB)
  • University of Cambridge (GB)
  • Rutgers, The State University of New Jersey (US)
  • Garvan Institute of Medical Research (AU)
  • University of Massachusetts Chan Medical School (US)
  • University of Geneva (CH)
  • Lawrence Berkeley National Laboratory (US)
  • Howard Hughes Medical Institute (US)
  • University of Chicago (US)
  • Institució Catalana de Recerca i Estudis Avançats (ES)
  • Max Delbrück Center (DE)
Corresponding author
  • Marlétaz, Ferdinand
  • Nakamura, Tetsuya
  • Tena, Juan J.
  • Lupiáñez, Darío G.
  • Rokhsar, Daniel S.
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2023-04-12
Volume
616
Issue
7957
Pages
495-503
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/s41586-023-05868-1
PMC
PMC10115646
OpenAlex
W4365143664
Cited by
71
References
7
Citations by year
2026: 17 · 2025: 23 · 2024: 15 · 2023: 13 · 2022: 3
FWCI
5.87
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (publishedVersion)
  • MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
  • Okinawa Institute of Science and Technology Graduate University (Okinawa Institute of Science and Technology Graduate University) (submittedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • UCL Discovery (University College London) (submittedVersion, cc-by)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • ResearchSpace (University of Auckland) (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion)
Funders
  • National Science Foundation (DEAC02-05CH11231, 2210072)
  • Howard Hughes Medical Institute (DE-AC02-05CH11231)
  • U.S. Department of Energy (-AC02-05CH11231, 05CH11231, DE AC02 05CH11231, DE-AC02-)
  • Royal Society (DE-AC02-05CH11231, URF\R1\191161)
  • Deutsche Forschungsgemeinschaft (EMBO ALTF 537-2020, DE-AC02-05CH11231)
  • Ministerio de Economía y Competitividad (PID2019, DE AC02-05CH11231, PID2019-103921GB-I00, PID2020)
  • Junta de Andalucía (DOC_00397)
  • National Institutes of Health (DE-AC02–05CH11231)
  • Biotechnology and Biological Sciences Research Council (BB/V01109X/1)
  • National Human Genome Research Institute (R01HG003143, R01HG003988)
  • National Institute of Dental and Craniofacial Research (R01DE028599)
  • Lawrence Berkeley National Laboratory (AC02‐05CH11231, DE-AC02-05CH11231, R01HG003988, 05CH11231)
  • H2020 European Research Council (740041)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
little skate, Leucoraja erinacea, HOXA genes, enhancer evolution, microchromosomes, genome rearrangement, fin development, chromatin occupancy, 3D genome organization, phenotypic innovation, jawed vertebrates
MeSH terms
Animals, Biological Evolution, Skates, Fish, Zebrafish, Genome, Genes, Reporter, Homeodomain Proteins, Genomics, Animal Fins

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