Abstract
Spiders are renowned for their ecological versatility and silk-based innovations in materials science, yet marine environments remain virtually uncolonized by this predominantly terrestrial lineage. A striking exception is the obligate intertidal spider genus Desis, whose members have evolved extraordinary physiological and behavioural adaptations to persist in wave-swept, saline habitats that oscillate between land and sea. However, the molecular basis of these adaptations has remained largely unexplored. Here, we present a high-quality, chromosome-scale genome of the intertidal spider Desis jiaxiangi, together with a reference genome of the water spider Argyroneta aquatica, integrated with transcriptomic and proteomic data. This multi-omics framework reveals the genomic architecture underlying adaptation to life at the ocean's edge. We uncover expansions of gene families linked to hormone biosynthesis and DNA repair, alongside signatures of adaptive evolution in genes involved osmoregulation, the rate-limiting step of glycolysis, mitochondrial regulation, epithelial tube morphogenesis and circadian rhythm. Notably, we characterize a novel silk spidroin enriched with a unique GVGAKV motif, which may enhance silk hydrophobicity, and detect the duplication burst of hemocyanin genes likely supporting oxygen transport during submersion. Together, these findings reveal convergent molecular strategies for coping with extreme and fluctuating environments, and demonstrate how genomic innovation enables terrestrial lineages to invade marine-influenced ecosystems. Our study establishes Desis as powerful model for understanding adaptation at terrestrial-marine interface.