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

Lead Research Organisation: University of Bristol
Department Name: Biological Sciences

Abstract

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.

Technical Summary

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.

Planned Impact

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.

Publications

10 25 50
 
Description 2020:
Work Packages 1 and 2 are complete with one WP2 manuscript published and three additional manuscripts nearing completion related to Evolution of photoreceptors in Sabellids, sabellid phylogenetics, and neuroanatomy. Lab work regarding behavioural responses of fan worms to visual stimuli have been extremely successful, with the final trials to be completed by early April.

We have made significant discoveries regarding the unique evolutionary story of the radiolar eyes in the fan worms. The eyes have evolved independently in essentially every genus and make use of a divers array of optical strategies. This work highlights the extreme creativity of evolutionary processes, seizing on a number of unique approaches to solve a single sensory problem.

2019:
In the first half of my FLF, I have made significant progress on Objectives 1 and 2 of my proposal, related to transcriptomic sequencing of fan worm radiolar eyes, and characterising the neural pathways that that communicate visual information to the brain.

Towards Objective 1, I have successfully completed field trips and collected over 30 unique species of these worms, with varying complexities of radiolar eyes. High quality RNA has been extracted from the tissue and 17 species have been submitted to Illumina transcriptomic sequencing. The resulting sequence data has been analysed for phototransduction components and a manuscript is in progress. Further sequencing is being performed by international collaborators to contribute to a second manuscript on the phylogenetics of the group synthesised with my previous transmission electron microscopy data on photoreceptor structures. In total, this dataset will help to explain the unique evolutionary and developmental history of these unusual eyes.

Towards Objective 2, I have successfully complete a set of electroretinogram experiments that have characterised the light sensitivity characteristics of the eyes in my focal species, Acromegalomma vesiculosum. A publication is ready for submission for this work and it will further inform the design of behavioural experiments for Objective 3. Also towards objective 2, I have completed microCT scans of the brains of my focal species; one with large, consolidated eyes, one with small distributed eyes, and one without eyes. I have also added finer detail to these observations with beamline time at the Diamond Light Source synchrotron. The reconstructions of the CNS in these species will be coupled with photoreceptor projection tracing by neurobiotin injection into the eyes in order to understand the first order neuronal wiring, to be undertaken this summer. I have also completed Biodian staining histology of the brain in each of these species, and have identified the visual processing centers and other major sensory integration structures in the brain associated with the giant axons that control the retraction response.

Towards Objective 3, I have set up lab aquaria containing a stable population of two focal species that will be used for behavioural experiments that will be informed by the results of Objective 2. Preliminary behavioural tests have been carried out, the methodology is designed, and the testing arenas are now constructed. Experiments will progress in the coming year.

I have initiated collaboration with an EPSRC Innovation Fellow, László Tálas, to begin computational analysis of the fan worm visual system. Using my underwater light field measurements from fan worm habitats and tomographic 3D reconstructions of the various fan worm eye types, László is developing 3D simulations of various fan worm eye types and visual stimuli. This will allow us to test hypotheses about these unique visual processing circuits drawn from the findings in Objectives 2 and 3. Such computational models are the ultimate final objective of this proposal.
Exploitation Route The transcriptomic dataset form Objective 1 will be of interest to polychaete ecologists and systematics taxonomists, as well as those interested in the evolution and development of sensory systems. Objective 2 and 3 will ultimately be of interest to neuroethologists and synthetic sensory processing researchers.
Sectors Electronics,Manufacturing, including Industrial Biotechology,Other

 
Description (PhoToBe) - New ways from photon to behaviour: Finding new phototransduction cascades in fan worms
Amount € 212,933 (EUR)
Funding ID 846655 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 01/2020 
End 12/2021
 
Description Electrophysiological recordings from fan worm radiolar eyes. 
Organisation University of Copenhagen
Country Denmark 
Sector Academic/University 
PI Contribution Collection of fan worms, Acromegalomma vesiculosum, and carrying out ERG experiments.
Collaborator Contribution Training and use of electrophysiological ERG equipment.
Impact We have obtained visual electrophysiological recordings from the fan worms describing their light responses, spectral sensitivity, and flicker fusion frequency. A publication stemming from this collaboration is in preparation and the finding will contribute to objectives 2 and 3 of the proposal. The collaboration is multidisciplinary and involves visual ecology and neurobiology.
Start Year 2018
 
Description Neuroanatomy of Fan Worms 
Organisation University of Maryland Baltimore County
Country United States 
Sector Academic/University 
PI Contribution Provided prepared specimens.
Collaborator Contribution Chan Lin has hosted me in his lab to preform Bodian neural stains of four species of fan worms: Including a two-eyed species, a many-eyed species, and eyeless species.
Impact These stainings have identified the relevant visual processing centers in the brain and will contribute towards a manuscript.
Start Year 2018
 
Description Phylogenetics of sabellid fan worms 
Organisation Norwegian University of Science and Technology (NTNU)
Country Norway 
Sector Academic/University 
PI Contribution Collection of taxonomic specimins from 40 species of fan worms.
Collaborator Contribution Identification of fan worm species and assistance with constructing a new phylogeny of sabellids incorporating sequencing data from Objective 1 in collaboration with University of Hawai'i at Manoa.
Impact Collaboration is in progress. This collaboration is multidisciplinary and incorporates systemics, taxonomy, and molecular phylogenetics.
Start Year 2017
 
Description Transcriptomic sequencing of fan worm radiolar eyes 
Organisation University of Hawai'i at Manoa
Country United States 
Sector Academic/University 
PI Contribution Collection of fan worms, dissection, and fixation of radiolar eyes.
Collaborator Contribution RNA extraction from the radiolar eyes of 20 species of fan worms for submission to transcriptomic sequencing. Analysis of resulting data will fulfill Objective 1 of the proposal.
Impact Collaboration is ongoing and outputs will be generated following completion of transcriptomic sequencing. This collaboration is multidisciplinary and incorporates developmental biology, phylogenetics, and bioinformatics.
Start Year 2017
 
Description Visual ecology of the thrips pest insect 
Organisation Lincoln University
Country New Zealand 
Sector Academic/University 
PI Contribution Under this collaboration, I am hosting a PhD student (Karla Lopez Reyes) from Lincoln University. I am advising and assisting her with anatomical, molecular, and optical studies of the eye of the Western Flower Thrips, Frankliniella occidentalis. These studies will inform the design of new traps for the control and monitoring of this important agricultural pest.
Collaborator Contribution Monetary support and student lab work following up preliminary results I generated previously.
Impact The collaboration research initiated in January 2019 and has not yet produced outcomes.
Start Year 2018
 
Description International Workshop: Light Environment and Visual World of Animals. SOKENDAI, Japan 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact A workshop to disseminate new environmental light measurement techniques developed by myself, Dan-Eric Nilsson (Lund University) and others to researchers at SOKENDAI Institute, Japan.
Year(s) Of Engagement Activity 2019
 
Description Lecture on the intersection of science and art in photography for Art History Undergraduate course. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Lecture on the intersection of science and art in photography for Art History Undergraduate course.
Year(s) Of Engagement Activity 2019
 
Description Science Exploration Education (S.E.E) Initiative and Open Explorer Expeditions. 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I successfully applied for and received an submersible ROV from the National Geographic Science Exploration Education (S.E.E) Initiative. The ROV is being used for natural behavioural monitoring of my fan worm study species as well as for underwater environmental light measurements. Some observations made with this equipment are reported on the National Geographic Open Explorer expeditions portal in to form of blog posts aimed at science and nature enthusiasts in the general public. I also plan to use the ROV for engagement with schools near my field site in Cornwall in collaboration with the Helford Voluntary Marine Conservation Society.
Year(s) Of Engagement Activity 2019
 
Description Speaker at Bristol Neuroscience Festival 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Bristol Neuroscience Festival outreach event.
Year(s) Of Engagement Activity 2020