Insights into vertebrate electroreceptor evolution from the lamprey lateral line

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Our sense of hearing, and the information we use for balance, results from the movement of tiny 'hairs' on sensory 'hair cells' in our inner ears, in response to fluid motion within the inner ear. In fish and amphibians, hair cells are also found on the body surface, in sense organs ('neuromasts') arranged in lines over the head and body. These 'lateral line' hair cells detect local water flow ('touch at a distance'). Many fish and amphibians (e.g., sharks, sturgeons, salamanders) also have electrosensory lateral line organs that detect the weak electric fields around animals in water (primarily used for hunting live prey). In electroreceptive fish and amphibians, both types of sense organ, plus the neurons (nerve cells) that transmit information from hair cells and electroreceptors to the brain, develop from embryonic 'lateral line placodes' (patches of thickened skin on the head). Electroreception is an ancient sense, as old as the vertebrates. We know this because lampreys, from the only surviving lineage of jawless vertebrates, are electroreceptive. Lamprey electroreceptors seem to work in the same way as those in jawed vertebrates, and the same lateral line nerve (the anterior nerve) transmits their information to the same specialised part of the brain as in electroreceptive jawed vertebrates, suggesting this system was present in the common ancestor of all living vertebrates. How did electroreceptors evolve? We previously showed that bony fish electroreceptors are closely related to hair cells. For example, we found that 'transcription factor' genes (encoding proteins that control the activity of other genes) required for hair-cell formation are also active in developing ampullary organs. This suggests that electroreceptors likely evolved from lateral line hair cells. Uniquely, lateral line nerves in the lamprey are also needed for a reflex swimming response away from light. In lampreys, therefore, the lateral line system includes 'photoreceptor' cells that respond to light, as well as 'mechanoreceptors' (hair cells) that respond to local water movement, and electroreceptors that respond to electric fields. Light sensitivity has not been reported in the lateral line of jawed vertebrates, but several recent studies reported the expression of genes encoding opsins, which can detect light, in zebrafish neuromasts, including in hair cells. So, it is possible that some or all lamprey neuromast hair cells may be light-sensitive, as well as responding to water movement.In this grant proposal, we aim to shed light both on electroreceptor evolution and on the light-avoidance swimming reflex, by studying the development of hair cells, electroreceptors and photoreceptors (which may be hair cells) in embryos and larval stages of the sea lamprey. If electroreceptors evolved in the common ancestor of all living vertebrates, we would expect lamprey electroreceptors to develop from lateral line placodes and to express similar genes as in jawed-vertebrate electroreceptors. To test this, we will inject vital fluorescent dyes to follow the development of the lateral line placodes and the projections of the lateral line nerves (only the anterior lateral line nerve innervates electroreceptors, including those on the trunk); study the expression of genes known to be active in jawed-vertebrate electroreceptors, and the opsin genes reported in zebrafish neuromasts; and take an unbiased 'single-cell' sequencing approach to identify novel genes expressed by each receptor cell-type. Finally, we will use CRISPR to mutate some of these genes, to determine whether they are important for the formation of electroreceptors or the function of photoreceptors.Overall, this work will yield the first information on lamprey lateral line receptor-cell development, identify the cellular and molecular basis of the enigmatic lateral line-mediated light-avoidance reflex, and shed light on the evolution of vertebrate sensory receptor cells.