Collective behavior emerges from genetically controlled simple behavioral motifs in zebrafish

Since Darwin, coordinated movement of animal groups has been believed to be essential to species survival, but it is not understood how changes in the genetic makeup of individuals might alter behavior of the collective. Here we find that even at the early larval stage, zebrafish regulate their proximity and alignment with each other. Two simple visual responses, one that measures relative visual field occupancy and the other global visual motion, suffice to account for the group behavior that emerges. We analyze how mutations in genes known to affect social behavior of humans perturb these simple reflexes in larval zebrafish and thereby affect their collective behaviors. We use model simulations to show that changes in reflexive responses of individual mutant animals predict well the distinctive collective patterns that emerge in a group. Hence group behaviors reflect in part genetically defined primitive sensorimotor “motifs”, which are evident even in young larvae.Long AbstractCoordinated movement of animal groups is essential to species survival. It is not clear whether there are simple interactions among the individuals that account for group behaviors, nor when they arise during development. Zebrafish at the early larval stage do not manifest obvious tendencies to form groups, but we find here that they have already established mechanisms to regulate proximity and alignment with respect to their neighbors, which are the two key ingredients of shoaling and schooling. Specifically, we show that two basic reflexes are sufficient to explain a large part of emerging collective behaviors. First, young larvae repel away from regions of high visual clutter, leading to a dispersal of the group. At later developmental stages, this dispersal reflex shifts to attraction and aggregation behaviors. Second, larvae display a strong tendency to move along with whole field motion stimuli, a well-described behavior known as the optomotor reflex (OMR). When applied to individuals swimming within a group, this reflex leads to an emergence of mutual alignment between close neighbors and induces collective motion of the whole group. The combined developmental maturation of both reflexes can then explain emergent shoaling and schooling behavior.In order to probe the link between single genetic mutations and emergent collective motion, we select fish with mutations in genes orthologous to those associated with human behavioral disorders and find that these mutations affect the primitive visuomotor behaviors at a very young age and persist over development. We then use model simulations to show that the phenotypic manifestations of these mutations are predictive of changes in the emergent collective behaviors of mutant animals. Indeed, models based solely on these two primitive motor reflexes can synergistically account for a large fraction of the distinctive emergent group behaviors across ages and genetic backgrounds. Our results indicate that complex interactions among individuals in a group are built upon genetically defined primitive sensorimotor “motifs”, which are evident even in young larvae at a time when the nervous system is far less complex and more directly accessible to detailed analysis.