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Ancestral photoreceptor diversity as the basis of visual behaviour

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From Nature Ecology & Evolution

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Abstract

Animal colour vision is based on comparing signals from different photoreceptors. It is generally assumed that processing different spectral types of photoreceptor mainly serves colour vision. Here I propose instead that photoreceptors are parallel feature channels that differentially support visual-motor programmes like motion vision behaviours, prey capture and predator evasion. Colour vision may have emerged as a secondary benefit of these circuits, which originally helped aquatic vertebrates to visually navigate and segment their underwater world. Specifically, I suggest that ancestral vertebrate vision was built around three main systems, including a high-resolution general purpose greyscale system based on ancestral red cones and rods to mediate visual body stabilization and navigation, a high-sensitivity specialized foreground system based on ancestral ultraviolet cones to mediate threat detection and prey capture, and a net-suppressive system based on ancestral green and blue cones for regulating red/rod and ultraviolet circuits. This ancestral strategy probably still underpins vision today, and different vertebrate lineages have since adapted their original photoreceptor circuits to suit their diverse visual ecologies.

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Fig. 1: Hypothesis and definition of vertebrate photoreceptors.
Fig. 2: Retinal architecture across species.
Fig. 3: Cones as feature channels.
Fig. 4: Inner retinal layering and spectral sensitivity functions of visual behaviours.

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Acknowledgements

I thank D. E. Nilsson, A. Kelber, J. Corbo, E. Mitchell, S. Laughlin, G. Jekeley, C. Yovanovich, K. Donner, C. Fornetto, D. Schoppik, P. Martin, T. Yoshimatsu, T. Euler, N. Hart, S. Collin and many others for inputs on some of the concepts elaborated in this article. Funding was provided by the Wellcome Trust (Investigator Award in Science 220277/Z20/Z), the European Research Council (ERC-StG ‘NeuroVisEco’ 677687), UKRI (BBSRC, BB/R014817/1 and BB/W013509/1), the Leverhulme Trust (PLP-2017-005, RPG-2021-026 and RPG-2-23-042) and the Lister Institute for Preventive Medicine. This research was funded in part by the Wellcome Trust (220277/Z20/Z). For the purpose of Open Access, the author has applied a CC BY public copyright licence to any author accepted manuscript version arising from this submission.

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    Tom Baden

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Baden, T. Ancestral photoreceptor diversity as the basis of visual behaviour. Nat Ecol Evol 8, 374–386 (2024). https://doi.org/10.1038/s41559-023-02291-7

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