Algal metabolites effect on sea urchins: Reproductive disruption as a possible driver of coevolution

Chemical defenses shape ecological interactions across marine food webs, yet their reproductive and evolutionary consequences in macroalgae-grazer systems remain largely unexplored. Here, we integrate physiological, developmental and molecular assays to investigate how secondary metabolites from two brown algae, Ericaria brachycarpa and E. crinita, modulate reproduction and early development of their natural grazer sea urchin Arbacia lixula. The oxylipin-containing extract of E. brachycarpa (EBE) caused severe, dose-dependent impairment of fertilization and embryogenesis, whereas the meroterpenoid-rich extract from E. crinita (ECE) showed no detectable effects. Adult urchins tolerated both extracts except for the EBE highest concentration, suggesting detoxification or compensatory stress-response mechanisms. On contrast, gametes were markedly sensitive, exhibiting complete chromatin fragmentation with sperm being the most vulnerable target. Embryos exposed to low doses showed a general delay in development, while the highest doses caused developmental arrest and apoptotic features. Strikingly, EBE induced a novel phenotype characterized by the formation of an extra embryonic membrane, likely acting as a defensive mechanism. Parental exposure did not affect offspring development, indicating that toxicity acts primarily through direct exposure rather than inherited stress responses. Western blot analyses revealed a marked modulation of cellular stress markers (HSP60, HSP70, LC3, p62, cleaved caspase-7), showing sex-specific responses in gonads and the activation of apoptotic pathways in gametes. Our findings provide the first experimental evidence that macroalgal oxylipins can act as potent natural reproductive inhibitors, selectively targeting early life stages and representing a mechanism shaping grazer-alga coevolution and influencing the renewal, resilience and trophic balance of Mediterranean coastal ecosystems.