Molecular Drivers of Mutualistic Association Between Anemone and Anemonefish

The anemone-anemonefish mutualism is one of the most iconic in the marine environment. While the evolution of this mutualistic relationship has contributed to the ecological success of both partners, the underlying molecular processes that establish and maintain it remain poorly understood, particularly how anemonefish tolerate anemone venom. Here, we characterize the transcriptional dynamics in both the anemonefish Amphiprion clarkii and its host anemone Entacmaea quadricolor 48 h after association, providing a rare insight into the coordinated molecular processes in both partners that underlie symbiosis establishment. Upon acclimation with an anemone, anemonefish showed differential regulation of sensory perception and memory genes in key brain regions, indicating activation of neural pathways that may facilitate host recognition and mutualism establishment. In the fish's skin, altered expression of genes involved in neurotransmitter release, cytoskeleton organization, and venom receptor proteins points to mechanisms of resistance to anemone venom. This resistance is particularly remarkable since anemone hosting fish exhibited increased expression of genes encoding mechanoreceptors, putative venom-associated proteins, and ion channels involved in nematocyst discharge, indicating the anemone does indeed mount an active response to their mutualistic partner. By simultaneously capturing the molecular responses of both symbiotic partners, our results reveal the complex, coordinated interplay of molecular events in both species that play a pivotal role in establishing this mutualistic relationship.