Looking with gills: The evolution and function of distributed visual systems in fan worms with a view to future resilient sensor arrays

We are often fascinated to ponder how other animals see the world. Since most creatures have two primary eyes positioned prominently on the head, we are generally able to imagine some derivation or elaboration of our own view. However, there are some cases in which the visual system departs so wildly from ours that it is difficult to conceive how such a system would function, let alone provide the animal with useful information about the world. Marine fan worms possess arguably the most bizarre visual system in nature. These worms spend their lives within tubes on the sea floor, and project their eponymous fans, composed of numerous tentacles called radioles, up into the water column. These radioles are responsible for filter feeding, respiration, and amazingly - vision. In many species, the radioles are covered with variable arrangements of eyes; sometimes scattered in the hundreds on all of the radioles, other times consolidated into a pair of large compound eyes on the tips of two radioles, and in almost any arrangement in-between. These eyes likely function as a sort of optical burglar alarm, detecting the movement of looming threats and stimulating a rapid withdrawal into the fortified tube. My research has suggested that these radiolar eyes represent a completely novel evolutionary development, using light-sensing genes and neural pathways unlike those in the eyes of any other animal. These features make fan worms a spectacular study system to explore the origins of vision and the development of complexity and organization in distributed visual sensory systems.

I propose to investigate the evolution and function of radiolar eyes in fan worms using molecular, neurobiological, and computational approaches. Next-generation sequencing techniques will be used to identify the genes involved in light detection and phototransduction, as well as developmental cues that give rise to the variable arrangements of eyes observed in different species of fan worms. I will also trace neuronal projections from the eyes to the brain in order to understand how information from a seemingly-chaotic, distributed array of eyes or ocelli is integrated and interpreted in order to stimulate a reliable startle response. Ultimately, I will draw upon these investigations in order to produce a synthetic model for simple, redundant, distributed optical sensory arrays that will have implications to biomimetic robotics.

Marine fan worms possess some of the most unusual eyes in nature. These sessile polychaetes spend their lives within tubes and project their eponymous fans, made up of two sets of branchial tentacles called radioles, up into the water column. These radioles are responsible for filter feeding, respiration, and amazingly - vision. In many species, the radioles are covered with variable arrangements of ocelli or even elaborate compound eyes; sometimes scattered in the hundreds on all of their radioles, and other times consolidated into a pair of large compound eyes on the tips of two radioles. The radiolar eyes likely function as optical burglar alarms, detecting the movement of looming threats and stimulating a rapid withdrawal response into the tube. My research has shown that the remarkable diversity of radiolar eyes in fan worms likely arose more than once in evolutionary history form phototransduction components and neural circuits that are not involved in canonical visual systems. These features make fan worms a spectacular study system to explore the origins of vision and the development of complexity and organization in distributed visual sensory systems.

I propose to investigate the evolution and function of radiolar eyes in fan worms using molecular, neurobiological, and computational approaches. I will preform transcriptomic sequencing of radioles from species bearing a variety of eye types to identify expressed phototransduction and developmental genes. I will trace neuronal projections from the eyes to the brain in order to understand how information from a seemingly-chaotic, distributed array of eyes or ocelli is integrated and interpreted in order to stimulate a reliable startle response. Ultimately, I will draw upon these investigations in order to produce a synthetic model for simple, redundant, distributed optical sensory arrays that will have implications to biomimetic robotics.

Who might benefit from this research?

There are numerous beneficiaries from this research. Ultimately the results and data generated have the potential to enable impact and innovation for a broad range of disciplines.

Academic beneficiaries come from areas in the biosciences such as sensory biology, behavioral ecology, evolutionary biology, phylogenetics and evo-devo. The work will also reach fields in engineering, such as machine and computational vision and network design. Researchers interested in the process of regeneration and neural plasticity (healthy ageing) in new model systems will benefit from data generated. This project also represents the first steps towards developing distributed network systems. The future of search and rescue, and environmental and health monitoring will involve optimized, simple, and resilient distributed networks. Through this project, a better understanding of an evolutionary optimized distributed visual system in fan worms will act as bio-inspiration for these fields.

Moreover, researchers, such as myself, who are involved in the project will benefit from the new skills and collaborations that will be developed. This in turn increases the level of UKs science base that will essentially benefit the UK bio-economy.

How might they benefit from this research?

Academic Impact: The data that I will generate regarding a naturally-evolved distributed optical sensory array in fan worms will provide a unique perspective on a novel means of creating resilient biomimetic analogs. Beyond this, a truly wide breadth of biological researchers wide will find long-term relevance in the data, and publications I generate. The normal routes of seminars, peer reviewed publications and conferences will be used to disseminated my work. Furthermore, I am committed to the public dissemination of science and will continue to communicate my discoveries through public talks, social media and public science events such as the Festival of Nature.

Bio-economic impact: The UK bio-economy relies on highly skilled individuals, knowledge generation and the training future leaders to drive forward research that will develop future impact. During this fellowship I will be able to benefit from the associated training that will enhance my research profile, the CPD courses in leadership and research management that Bristol offers and the mentorship that both Bristol and the BBSRC provide.

Translation: In discovering how this resilience is utilized in the novel, distributed vision systems there is translational potential to technological control systems for man-made networks. In order to protect any IP that is generated, I will liaise with the Research and Development team at Bristol to monitor any commercial opportunities that may arise.