Abstract

Choanoflagellates, the closest living relatives of animals, can form multicellular colonies of various shapes and sizes. This diversity and the simplicity of multicellular forms in conjunction with their important phylogenetic position makes choanoflagellates an ideal system for studying the evolution of morphogenesis. Comparisons between the biology of choanoflagellates and animals has begun to shed light on animal origins. However, because most work has focused on genetics and genomics, little is known about the cellular and biophysical mechanisms underlying the regulation of multicellular form in choanoflagellates. Through the quantitative characterization of the biophysical processes underlying the development of rosette colonies in the choanoflagellate Salpingoeca rosetta, we found that rosettes reproducibly transition from 2D-3D growth, despite the underlying stochasticity of the cell lineages. We postulated that the extracellular matrix (ECM) exerts a physical constraint on the packing of proliferating cells, thereby sculpting morphogenesis. Perturbative experiments coupled with biophysical simulations demonstrated the fundamental importance of a basally-secreted ECM for rosette morphogenesis. In addition, this yielded a morphospace for the shapes of multicellular colonies, consistent with observations across a range of choanoflagellates. Overall, our biophysical perspective complements previous genetic perspectives and thus helps illuminate the interplay between cell biology and physics in regulating morphogenesis. Another choanoflagellate, the recently discovered Choanoeca flexa, forms multicellular cup-shaped colonies. Colonies rapidly invert their curvature in response to changing light levels, which they detect through a rhodopsin-cGMP pathway. Inversion is mediated by cell shape changes requiring actomyosin-mediated apical contractility and allows alternation between feeding and swimming behavior. C. flexa thus rapidly converts sensory inputs directly into multicellular contractions. In this respect, it may inform reconstructions of hypothesized animal ancestors that existed before the evolution of specialized sensory and contractile cells.