Transient Leadership and Collective Cell Movement in Early Diverged Multicellular Animals

Our work tackles collective motion and decision-making in a primitive multicellular animal, Trichoplax adhaerens, enabling pioneering research into how intercellular coordination affects animal behavior and how migration accuracy scales with group size. Collective motion of cells is critical to some of the most vital tasks including wound healing, development, and immune response [Friedl and Gilmour 2009; Tokarski et al. 2012; Lee et al. 2012; Beltman et al. 2009], and is common to many pathological processes including cancer cell invasion and teratogenesis [Khalil and Friedl 2010]. The extensive understanding of movement by single cells [Rørth 2011; Insall and Machesky 2011; Houk et al. 2012] is insufficient to predict the behavior of cellular groups [Theveneau et al. 2013; Trepat, X. and Fredberg 2011], and identifying underlying rules of coordination in collective cell migration is still evasive. This is of particular interest, as collective motion and decision-making are fundamental phenomena in systems ranging from molecules [Schaller and Bausch 2013] to animal societies [Couzin et al. 2005], and recent studies evidence the existence of common mechanisms among disparate systems, such as group polarization by chase-and-run in neural crest cells and marching locusts [Theveneau et al. 2013; Bazazi et al. 2008]. Few of the supposed benefits of collective motion have ever been tested at the cellular scale. As an example, though collective sensing allows for larger groups to exhibit greater accuracy in navigation [Simons 2004; Berdahl et al. 2013] and group taxis is possible through the leadership of only a few individuals [Couzin et al. 2005], such effects have never been investigated in collective cell migration. It has also proven difficult to relate observed phenomena to animal behavior and fitness.