Active flow sensing during helical swimming in a ciliary microswimmer

This fundamental research project will develop a new systems-level understanding of a miniature nervous system in a marine larva and how it functions in aquatic habitats with dynamic fluid flows. It proposes an interdisciplinary research framework that tightly integrates biological and physical thinking and approaches. The ability for aquatic animals to sense and respond to the movement of water around them can be important for survival. For example, fish can detect flows generated by the movement of other fish, and this sense allows them to form large schools. Other aquatic animals are able to evade approaching predators such as jellyfish by sensing the flow perturbations generated by the predator. Fish and other marine plankton can also sense the flow direction and reorient themselves to swim against the flow. This upstream swimming is known as rheotaxis, and is also the mechanism by which sperm cells navigate towards the egg for internal fertilization. How animals sense and respond to flow is incompletely understood. Organisms rely on an intricate coupling between the environmental stimulus, and their own self-movement. Our aim is to understand the neuronal and behavioural control of flow responses in a marine organism. We will study flow sensation in the larvae of a marine ragworm called Platynereis. Platynereis can be cultured in the laboratory and our team has established this animal for the experimental study of the neural mechanisms of zooplankton behaviour. We have recently discovered that the larvae of this ragworm have neurons that respond specifically to fluid flow. In this project, we will use advanced microscopy techniques to uncover how these neurons connect to the rest of the nervous system and data-driven computer modelling to reveal how flow sensation alters the larva's helical swimming behaviour. We will create custom chambers and arenas to test how single larvae respond to controlled fluid flows and microenvironments. Ragworm larvae measure only one fifth of a millimetre and this small size will allow us to investigate flow sensation at a level of detail that is not yet feasible for larger animals. Since Platynereis shows many neuronal and molecular characteristics that are similar to those found in vertebrates, our study will uncover general principles of flow sensation in animals.

The ability to sense velocity gradients or "shear" is widespread in aquatic organisms. Although flow-sensory neurons and their afferents have been described (e.g. in the lateral line of fish), we lack a whole-body understanding of the circuit mechanisms of sensing and responding to flow. In this project, we aim to obtain a systems-level description of flow sensation in the ciliated larvae of the marine annelid Platynereis dumerilii. In preliminary work, we identified flow sensory neurons in larval Platynereis. In this project, we aim to understand how these neurons function and connect to the rest of the larval nervous system and how larvae respond to shear flows. We aim to use behavioural, genetic and neurobiological experiments and computer simulations to characterise flow responses. By live imaging, we will investigate the responses of flow-sensory cells and their downstream circuits to dynamic flow signals. In microfluidics devices, we will characterise swimming trajectories. Flow responses will be analysed in wild-type larvae and larvae mutant for a conserved mechanosensory channel. To analyse the whole-body circuit of flow responses, we will use whole-body connectomics, calcium imaging and mathematical modelling of circuit dynamics. Based on the experimental results, we will develop a computer model of flow responses during helical swimming. This will deliver a comprehensive view of the nonlinear responses of a helical microswimmer to different flow fields and derive new predictions for experimental studies. We hypothesise a new mechanism of active shear sensing during helical swimming, similar to the mechanism of helical phototaxis by Platynereis and other larvae. The use of Platynereis as an experimentally tractable planktonic organism will allow us to investigate flow sensation at an unprecedented level of cellular and mechanistic detail. Our integrative approach promises to deliver a comprehensive model of flow sensation in an aquatic microswimmer.