Social-like responses are inducible in asocial Mexican cavefish despite the exhibition of strong repetitive behaviour

Abstract

Collective behaviors, such as schooling of fishes and mass migrations of ungulates, are hallmark features of a wide variety of animal species. Such phenotypic characters can be lost, either through evolutionary process across generations or by certain environmental stressors within a generation. Such stressors simultaneously promote stereotypic repetitive behaviors in many mammals, such as those exhibited in certain ex-situ captive settings. However, in asocial species, it is unclear whether social ability is permanently lost or only suppressed. It is also unclear if this antagonistic regulation between repetitive and social behaviors is deeply conserved among vertebrates. An evolutionary model, the Mexican tetra, Astyanax mexicanus, has a blind cave-dwelling morph lacking collective behaviors but exhibiting repetitive circling. In contrast, the sighted surface riverine morph of A. mexicanus shows more normative behaviors. We here report that social-like interactions are recoverable in blind asocial cavefish under familiar environments but are suppressed under the stress-associated unfamiliar environments. In contrast, surface fish revealed robust social-like behaviors in the dark, regardless of familiarity to the environment. Treatment of a human antipsychotic drug also induced social-like interactions in cavefish even in unfamiliar environments. In addition, the level of repetitive behavior is positively correlated with that of asociality in cavefish, suggesting that the antagonistic regulation between repetitive and social-like behaviors is present in teleost fish. Asocial cavefish therefore, with a deeply conserved framework of behavioral regulation, are still capable of expressing social-like behavior following ca. 200,000 years of adaptation to caves.