Hypoxia adaptation shapes genomic architecture and vertical niche transitions in copepods

Oxygen Minimum Zone (OMZ) expansion is a major challenge to marine ecosystems and associated zooplankton. Calanoid copepods include lineages that tolerate hypoxia and exhibit functional traits such as diel vertical migrations to, or dormancy within, hypoxic mesopelagic zones. However, the evolutionary origins and molecular drivers of these traits remain unclear. Herein, we integrate a time-calibrated phylotranscriptomic tree of 50 copepod species with ancestral trait reconstruction, gene family copy number variation, and palaeoceanographic data to infer the evolutionary timing and ecological drivers of hypoxia adaptation. Our results support that post-embryonic dormancy originated in calanoid ancestors, accompanied by widespread gene expansions primarily involving hypoxia-response pathways as well as lipid and amino acid metabolism. Mesopelagic colonisation by calanoid lineages likely occurred during the Ordovician deep-sea oxygenation event. This was followed, during the Carboniferous deep-sea deoxygenation, by a secondary habitat shift toward shallower waters and embryonic dormancy, and gene contractions in the superfamily Diaptomoidea. We further analysed the hypoxia-induced transcriptomic response of Eucalanus hyalinus from the Benguela upwelling OMZ, and identified a coordinated response involving extracellular matrix remodelling, amino acid recycling for anaerobic energy and antioxidant production as well as triglycerides to wax ester conversion. Gene family expansions upstream (proteolysis, transport) and downstream (antioxidant biosynthesis) of core metabolic pathways suggest purifying selection on dosage-sensitive nodes. Together, these results link palaeoclimate change to lineage-specific genome evolution patterns supporting copepod adaptation to oxygen limitation.