The emergent Yo-yo movement of nuclei driven by collective cytoskeletal remodeling in pseudo-synchronous mitotic cycles

Many aspects in tissue morphogenesis are attributed to the collective behavior of the participating cells. Yet, the mechanism for emergence of dynamic tissue behavior is not understood completely. Here we report the “yo-yo”-like nuclear drift movement in Drosophila syncytial embryo displays typical emergent feature of collective behavior, which is associated with pseudo-synchronous nuclear division cycle. We uncover the direct correlation between the degree of asynchrony of mitosis and the nuclear collective movement. Based on experimental manipulations and numerical simulations, we find the ensemble of spindle elongation, rather than a nucleus’ own spindle, is the main driving force for its drift movement. The cortical F-actin effectively acts as a viscoelastic material dampening the drift movement and ensuring the nuclei return to the original positions. Our study provides insights into how the interactions between cytoskeleton as individual elements leads to collective movement of the nuclear array on a macroscopic scale.