Hypoxia adaptation shapes genomic architecture and vertical niche transitions in copepods

Abstract

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 towards, or dormancy within, hypoxic mesopelagic zones. However, the evolutionary origins and molecular drivers of these functional 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 the following scenario: 1. Post-embryonic dormancy probably originated in calanoid ancestors, accompanied by widespread gene expansions involving hypoxia-response pathways as well as lipid and amino acid metabolisms. 2. Mesopelagic colonisation by calanoid lineages likely occurred during the Ordovician deep-sea oxygenation event. 3. During the Carboniferous deep-sea deoxygenation, a secondary habitat shift would have occurred toward shallower waters and embryonic dormancy, and as well as a contraction of the size of gene families in the Diaptomoidae. We further analysed the transcriptomic response of Eucalanus hyalinus from the Benguela upwelling OMZ versus surface waters, 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. Ka/Ks analysis of gene family expansions upstream (proteolysis, transport) and downstream (antioxidant biosynthesis) of core metabolic pathways suggested purifying selection on dosage-sensitive genes. Together, these results link palaeoclimate change to lineage-specific genome evolution patterns supporting copepod adaptation to oxygen limitation.