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Abstract Limb function requires polarized anatomy across the dorsal-ventral (DV) axis, but it is unclear when the capacity for DV differentiation of paired appendages arose in evolution. Here we define ancestral DV patterning programs in the fins of fishes. We show that the orthologue of the limb dorsal determinant, Lmx1b, is required to establish dorsality in zebrafish pectoral fins and is regulated by a conservedLARMcis-regulatory hub. However,lmx1bbexpression in median fins is unaffected by removal of theLARM, suggesting its regulation is an evolutionary innovation specific to the paired appendages. Although we find theLARMis highly conserved across gnathostomes, we identify specific alteration of this region in hillstream loaches, fishes which naturally parallel “double-ventral” fin phenotypes observed inlmx1bbandLARMmutants. Altogether our findings indicateLARM-mediated dorsal identity is an ancestral feature of paired appendages that provide a prepattern for limb evolution and lineage diversification. 

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.