Linking organismal behavior and morphogenesis during larva-polyp transition in Nematostella vectensis

While it is known that animal behavior depends on morphology, it remains poorly understood whether and how organismal behavior impacts morphogenesis. During development, behavior emerges at different scales when cells differentiate and form specialized tissues and organs. Such emerging behaviors may include movement or electrical activity taking place on scales ranging from the cellular to the organismal level. Since development is a continuous process, these emerging behaviors have the potential to feed back on development. Indeed, some behaviors that emerge at the tissue and organ scale, in particular contractile behaviors, such as the beating of the developing heart, have been shown to generate mechanical forces that contribute to morphogenesis. Thus, morphology and behavior develop together, and may impact one another. However, this potential two-way relationship has not received much attention at the organismal scale. This is largely because simultaneously studying behavior and morphogenesis is complicated by the different spatiotemporal scales at which these processes take place. Furthermore, while in most species morphogenesis largely takes place during embryonic development, most organismal behaviors are expressed post-embryonically, when they primarily serve animal survival through interaction with the external environment. For these reasons, studying the link between organismal behavior and morphogenesis requires a system in which both processes take place at the same time, and at spatiotemporal scales that are not too far apart. In this thesis, I use the sea anemone Nematostella vectensis as a model organism to study the link between organismal behavior and morphogenesis. During a process called larva-polyp transition, Nematostella undergoes a simple morphogenetic change from a roughly ellipsoidal larva to a cylindrical polyp with oral tentacles, while simultaneously expressing distinct organismal behaviors such as cilia-based swimming, settlement, and muscle-driven body contractions. Using an imaging setup that allows tracking and monitoring of morphogenetic and behavioral changes at the organismal scale, I characterize the dynamics of larva-polyp transition in wild-type animals. Here, I find that the animals can change their size and shape both separately and simultaneously, and that animal settlement behavior correlates with elongation dynamics. While increase of organismal size largely depends on body cavity inflation by water uptake, change of animal shape requires tissue remodeling during which cells change shape and rearrange. Furthermore, pharmacological, mechanical, and genetic perturbations suggest an important role for muscular-hydraulics in both animal behavior and development. These findings suggest a mechanism in which short-term behavioral contractions generate mechanical forces that induce tissue remodeling on long time scales, thus indicating a potential role for animal behavior in driving morphogenesis