Genomic and transcriptomic analyses reveal the adaptation to semi-aquatic and aquatic life in spiders

Spiders are largely terrestrial, but some lineages have independently adapted to marine and freshwater habitats. Although physiological and behavioral traits supporting these evolutionary transitions have been characterized, the genomic basis of adaptation to aquatic and semi-aquatic habitats in spiders remains unclear. Here, we report a chromosome-level genome assembly for the aquatic spider Argyroneta aquatica. Comparative analysis of 22 spider species supports 2 independent transitions in semi-aquatic (∼56 Mya) and aquatic (∼44 Mya) lineages. The aquatic spider shows distinct respiratory morphology compared with terrestrial spiders, including anterior spiracles and denser tracheoles. Molecular evolution analyses identified lineage-specific shifts in selective constraint or evidence of positive selection linked to trachea development (eg Wnt-1, Catenin beta, TMEM234, Arp3), hypoxia response (eg Uqcrfs1, COX5B, SLC2A3), lipid metabolism (eg Pnliprp2, ND-ACP), and osmoregulation. In the semi-aquatic spiders (Desis spp.), we detected strengthened purifying selection or positive selection on genes involved in respiratory/energy metabolism (eg SdhD, SLC2A3) and ion transporters (eg. Slc24a5). Comparative results further indicate that the A. aquatica genome may harbor bacterial-origin genes homologous to ABC transporters (39 genes) and acyl-CoA dehydrogenases (ACADs; 21 genes), which may support metabolic or transport functions in the aquatic lineage. Transcriptomic and metabolomic profiling of A. aquatica under hypoxic challenge revealed metabolic reprogramming, including shifts in glycolytic and TCA intermediates and upregulation of genes that promote fatty-acid β-oxidation (eg Slc13a5, AACS), consistent with extended anoxia tolerance (>48 h). Overall, this work provides genomic resources and highlights genomic signatures associated with semi-aquatic and aquatic adaptation in spiders.