Relaxed selection and horizontal gene transfer fuel underwater adaptation in a water spider

Abstract

AbstractThe water spider (Argyroneta aquatica) exhibits remarkable adaptability to thrive in aquatic environments and represents the only spider species capable of spending its entire life underwater. While its physiological and behavioral adaptations had been characterized, the genetic basis of underwater adaptation in spiders remains a fascinating topic that is poorly understood at multi-omics levels. Here, wede novoassemble a chromosome-level, high-quality genome of the water spider. A comparative analysis of spider genomes indicates that water spider has elevated genome-wide rates of molecular evolution associated with relaxed selection, which caused by reduced effective population size during the transition from territorial to underwater lifestyle. Remarkably, we found that horizontal gene transfer (HGT) emerges as a pivotal evolutionary force facilitating the underwater adaptation in water spider. We observed significant differentiation between water spiders under normal oxygenic and hypoxic conditions by utilizing comparative transcriptomics and metabolomics, and identified genes associated with hypoxia response pathways, especially hypoxia-inducible factor 1 (HIF-1) signaling pathway. Notably, we determined that genes within regulation HIF-1 pathway underwent positive selection (such asMARK1,Glut1,Hkdc1, andHsp90b1) or gene expansions through HGT-acquired (such as ABC and ACAD gene families), enhancing the hypoxia adaptation of the water spider. Altogether, our study provides insights into the genomic signature of adaptive evolution and specific genetic changes that underpin the transition to water life in spiders.