Social modulation of activity and orientation fosters complex interactions in young zebrafish

Abstract

Zebrafish are an important model organism for investigating collective behavior and neuropsychiatric disorders due to attributes such as fast development, high genetic homology with humans and a rich behavioral repertoire. Social behavior in zebrafish emerges as early as twelve days post-fertilization, building toward diverse, coordinated, and complex adult interactions. Most studies on social phenotypes, including in zebrafish, have focused on adult animals and assess isolated traits such as aggression, boldness, or social memory, leaving the critical period of early development when sociality emerges and the mechanisms underlying social behavior establishment largely unexplored. We present here a behavior analysis pipeline that identifies features describing general locomotion and social behavior based on simple geometric criteria. We apply this analysis to pairs of freely interacting two-week-old zebrafish and characterize nascent social preference. We find that young zebrafish favor a specific range of inter-fish distances, creating a social space characterized by specific modulation of locomotion features. Through quantitative analysis and modeling, we show that this proximity behavior is largely established through a turning bias toward counterparts and a socially induced suppression of the variance in turning angles over broader ranges of inter-fish distances. Furthermore, we describe how proximity fosters engagement by young zebrafish in transient, complex short-range physical interactions that include various forms of inter-fish contacts, reminiscent of patterns described in adult animals. Our approach has broad applications for understanding the ontogeny of sociality and collective behaviors and describing subtle phenotypes associated with various human disorders.