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Genomic data are lacking for most Antarctic marine invertebrates, predicating our ability to understand physiological adaptation and specific life-history traits, such as longevity. The environmental stress response of the Antarctic infaunal clamLaternula ellipticais much diminished in older adult animals compared with younger juvenile individuals. However, the mechanism underlying this reduced capacity is unknown. In this study, we describe and analyse the genome ofL. ellipticaand use it as a tool to understand transcriptomic responses to shell damage across different age cohorts. Gene expression data were combined with reduced representation enzymic methyl sequencing to identify if methylation was acting as an epigenetic mechanism driving age-dependent transcriptional profiles. Our transcriptomic results demonstrated a clear bipartite molecular response inL. elliptica, associated with a rapid growth phase in juveniles and a stabilization phase in reproductively mature adults. Genes active in the response to damage repair in juvenile animals are silent in adults but can be reactivated after several months following damage stimulus; however, these genes were not methylated. Hence, the trigger for this critical and imprinted change in physiological state is, as yet, unknown. While epigenetics is likely involved in this process, the mechanism is unlikely to be methylation. 

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.