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.
We thank R. Schneider, D. Sherwood and the staff of the Marine Biological Laboratory Embryology course for providing laboratory space; L. Bertrand and the staff at Leica Microsystems for microscopy support; D. Remsen, S. Bennett, D. Calzarette, and the staff of the Marine Biological Laboratory and MBL Marine Resources Center for technical and animal husbandry assistance; A. Gillis for support and advice with RNA-seq and skate functional experiments; and A. Shindo for technical support of image analysis. T.N., D.N. and A.A. were supported by institutional support provided by the Rutgers University School of Arts and Sciences and the Human Genetics Institute of New Jersey, a Whitman Center Fellowship (Marine Biological Laboratory) and the National Science Foundation under grant no. 2210072. D.N. was further supported by the NIH-IRACDA funded INSPIRE program at Rutgers University; F.M. and D.S.R. by funding from the Okinawa Institute for Science and Technology; D.S.R. by the Marthella Foskett-Brown Chair in Computational Biology; D.G.L. and R.D.A. by a grant from the Deutsche Forschungsgemeinschaft (LU 242672-1) and by a Helmholtz ERC Recognition Award grant from the Helmholtz-Gemeinschaft (ERC-RA1045 0033); R.D.A. and C.P. by EMBO Postdoctoral Fellowships (EMBO ALTF 537-2020 and ALTF 346-2020, respectively); P.M.M.G. by a postdoctoral fellowship from Junta de Andalucía (DOC_00397); J.J.T. and J.L.G.-S. by the European Research Council (ERC, grant no. 740041) and the Spanish Ministerio de Economía y Competitividad (grant no. PID2019-103921GB-I00); J.D. by the NIH grant HG003143; F.M. by the Royal Society (URF\R1\191161); V.A.S. by a Wolfson College Junior Research Fellowship and Marine Biological Laboratory Whitman Early Career Fellowship; J.L.-R. by the Spanish Ministerio de Ciencia e Innovacion (PID2020-113497GB-I00); and A.V. and F.D. by NIH grants R01DE028599 and R01HG003988. Research conducted at the E.O. Lawrence Berkeley National Laboratory was performed under US Department of Energy contract DE-AC02-05CH11231, University of California. J.D. is an investigator of the Howard Hughes Medical Institute.
- evoltionary development biology
- evolutionary genetics
- genome evolution