Snakes have retinas unlike any other vertebrate—some blur the line between rod and cone cells, others have unusually thick or thin neural layers, and the variation across species is greater than in mammals, birds, or fish. Yet almost everything scientists know about vertebrate vision comes from studying those other groups. This project will map every type of neuron and its connections in the retinas of ten snake species, using single-nucleus gene sequencing and high-resolution 3D electron microscopy. It will also sequence the full set of genes expressed in the retinas of 20 snake species to trace how vision-related genes have evolved across the snake family tree. This is fundamental science. It will not produce a new medical device or camera sensor next year. But understanding how evolution reshapes a basic neural circuit—the retina—into such wildly different forms could eventually inform bio-inspired imaging systems or shed light on how neural diversity arises more broadly. Past fundamental work on vertebrate retinas, for instance, underpinned the design of modern digital cameras and retinal implants.
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This project will apply cutting edge analyses of snake retinas, to provide new insights into the diversity, function, and adaptive evolutionary plasticity of vertebrate vision. The diversity of functions performed by the nervous system depends on the variety of cells that compose it, and their specific patterns of connectivity for processing information. Vertebrate retinas are highly organised networks of neurons (signalling cells). All vertebrates share a deeply conserved, common retinal plan with five main varieties (classes) of neuron. However, the number of types of neurons within each class and their signal-transmission pathways vary among different vertebrate species, depending on their visual needs and evolutionary history. A great deal is known about the function and evolution of vertebrate retinas, but most of that knowledge comes from detailed studies of some mammals, fish and birds, with much less known about amphibians or reptiles. In this project, we will identify, for the first time, all types of neurons and their connectivity in the retinas of snakes. Background knowledge tells us that studying snakes is highly likely to provide novel results of much wider relevance for two main reasons: (i) because the eyes and retinas of snakes are very distinct from those of other vertebrates, including their closest living relatives (lizards). Snakes have many unusual features including a fuzzy distinction between rod and cone photoreceptor cells (with instances of unusual rod-like cones and cone-like rods), a unique double cone, and great variation in the relative thickness of the different layers of neurons in the inner retina; (ii) because the retinas of snakes are extremely diverse, being much more variable than those of other major groups of vertebrates. We will discover the full range of different types of neurons and their connectivity in the retinas of a range of snake species that we have selected based on their having diverse retinal architecture, different complements of rods and cones, different activity patterns (diurnal and nocturnal), and coming from different branches of the snake evolutionary (‘family’) tree. This will be achieved by undertaking two cutting edge analyses for 10 snake species: (i) single-nucleus transcriptomics (using gene sequences to identify neuron types for approximately 20–30 thousand retinal cells), and (ii) high-resolution 3D electron microscopy to physically map the connections among neurons for a small volume of retina. In addition, we will generate whole-retina transcriptomes (to obtain DNA sequences of all the genes expressed in a retina) for 20 snake species, and use these data to infer patterns and processes of the molecular evolution of genes involved in vision (in combination with similar data available from published whole-genomes for snakes). The transcriptomic data will also be used to generate new antibodies that can be labelled fluorescently, in order to visualise the position and connections of individual types of neurons in snake retinas. This highly innovative and audacious project will provide a leap in understanding of the function and evolutionary origin of the extreme retinal diversity seen in snakes. The project is a UK-Brazil collaboration by two of the leading experts on snake visual systems, in concert with expert technical support from colleagues in Germany. This team has recently worked together to generate pilot data on snake retinal neuron connectivity. This project will provide fundamental gains for the advancement of knowledge in visual neurosciences worldwide, and for joint UK-Brazil research.
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