Parallel genomic remodeling associated with independent terrestrialization events in arthropods

Abstract

The repeated transition from aquatic to terrestrial environments (terrestrialization) has shaped the evolutionary trajectory of many animal lineages, yet the genomic basis of this ecological shift remains incompletely understood. Arthropods, with multiple independent terrestrialization events, provide a powerful system to investigate whether parallel genomic changes underlie adaptation to land. Here, we present a phylum-wide comparative phylogenomic analysis of 309 arthropod species representing aquatic and terrestrial lineages, using gene family evolutionary dynamics and directional selection analyses to uncover shared genomic strategies associated with life on land. We identified thousands of orthogroups showing parallel expansions or contractions across the three main lineages that colonized land (Arachnida, Myriapoda, and Hexapoda), of which a significant proportion also exhibited lineage-specific shifts in selective pressure. Functional enrichment of these orthogroups revealed functional convergence on processes such as oxidative stress response, transmembrane transport, energy metabolism, exoskeleton formation, and moulting regulation. Notably, parallel evolution in aquaporins, solute carriers, cytochrome P450s, superoxide dismutases, and heat shock proteins suggests that a conserved terrestrialization toolkit underlies independent colonization events. Additionally, parallel remodeling of key developmental and immune signaling pathways highlights the role of regulatory and structural innovations in adapting to terrestrial challenges. Our results provide the first large-scale genomic evidence of parallel molecular evolution driving arthropod terrestrialization and emphasize the power of comparative genomics to reveal shared solutions to ecological transitions across deep evolutionary timescales.