Socially regulated developmental plasticity in the color pattern of an anemonefish

Abstract

Understanding the developmental basis of phenotypic plasticity is key to unraveling the origins of biodiversity. In coral reef fishes, color pattern changes during ontogeny can serve adaptive functions, yet the mechanisms and ecological contexts shaping these transitions remain largely unknown. Here, we investigated color pattern development in the tomato anemonefish (Amphiprion frenatus), which exhibits transient posterior white barring during early juvenile stages. We demonstrated that the timing of bar loss is plastic and modulated by the social environment, where juveniles cohabiting with adult conspecifics exhibited bar loss [~]24 days earlier than those isolated from adults. Through transcriptomic profiling, we identified gene expression changes implicating apoptosis- and autophagy-related pathways, as well as alterations in chromatophore development. Moreover, shifts in the expression of multiple thyroid hormone marker genes highlighted the potential neuroendocrinal integration of social cues that promoted bar loss. Ultrastructural analyses via transmission electron microscopy and in-situ assays indicated massive apoptosis of iridophores and associated dermal remodeling during the white-to-orange transition. The pharmacological inhibition of caspases delayed bar loss, confirming the functional role of programmed cell death. Behavioral trials revealed that adults responded differently to juveniles with/without the posterior bar, suggesting a role of transient barring in conflict avoidance during recruitment. Lastly, our evolutionary reconstruction of this plastic trait suggests that colony size is an important factor promoting this ontogenetic switch throughout anemonefishes. Our results provide compelling evidence for socially mediated plasticity in color pattern ontogeny with ecological and evolutionary implications for communication and species diversification in reef fishes.