Metabolic shift toward ketosis in asocial cavefish increases social-like affinity

Abstract

Social affinity and collective behavior are nearly ubiquitous in the animal kingdom, but many lineages feature evolutionarily asocial species. These solitary species may have evolved to conserve energy in food-sparse environments. However, the mechanism by which metabolic changes regulate social affinity is not well investigated. In this study, we used the Mexican tetra (Astyanax mexicanus), which features riverine sighted surface (surface fish) and cave-dwelling populations (cavefish), to address the impact of metabolic shifts on asociality and other cave-associated behaviors in cavefish, including repetitive turning, sleeplessness, swimming longer distances, and enhanced foraging behavior. After 1 month of ketosis-inducing ketogenic diet feeding, asocial cavefish exhibited significantly higher social affinity, whereas social affinity regressed in cavefish fed the standard diet. The ketogenic diet also reduced repetitive turning and swimming in cavefish. No detectable behavioral shifts were found regarding sleeplessness and foraging behavior, suggesting that other evolved behaviors are not regulated by ketosis. We further examined the effects of the ketogenic diet via supplementation with extragenic ketone bodies, revealing that ketone bodies are pivotal molecules associated with social affinity. Our study indicated that fish that evolved to be asocial remain capable of exhibiting social affinity under ketosis.