Evolution of neuronal cell classes and types in the vertebrate retina

Joshua Hahn, Aboozar Monavarfeshani, Mu Qiao, Allison H. Kao, Yvonne Kölsch, Ayush Kumar, Vincent P. Kunze, Ashley M. Rasys, Rose Richardson, Joseph B. Wekselblatt, Herwig Baier, Robert J. Lucas, Wei Li, Markus Meister, Joshua T. Trachtenberg, Wenjun Yan, Yi-Rong Peng, Joshua R. Sanes () and Karthik Shekhar ()
Additional contact information
Joshua Hahn: University of California, Berkeley
Aboozar Monavarfeshani: Harvard University
Mu Qiao: California Institute of Technology
Allison H. Kao: Harvard University
Yvonne Kölsch: Max Planck Institute for Biological Intelligence
Ayush Kumar: University of California, Berkeley
Vincent P. Kunze: National Eye Institute, National Institutes of Health
Ashley M. Rasys: University of Georgia
Rose Richardson: University of Manchester
Joseph B. Wekselblatt: California Institute of Technology
Herwig Baier: Max Planck Institute for Biological Intelligence
Robert J. Lucas: University of Manchester
Wei Li: National Eye Institute, National Institutes of Health
Markus Meister: California Institute of Technology
Joshua T. Trachtenberg: David Geffen School of Medicine at UCLA
Wenjun Yan: Harvard University
Yi-Rong Peng: UCLA David Geffen School of Medicine
Joshua R. Sanes: Harvard University
Karthik Shekhar: University of California, Berkeley

Nature, 2023, vol. 624, issue 7991, 415-424

Abstract: Abstract The basic plan of the retina is conserved across vertebrates, yet species differ profoundly in their visual needs1. Retinal cell types may have evolved to accommodate these varied needs, but this has not been systematically studied. Here we generated and integrated single-cell transcriptomic atlases of the retina from 17 species: humans, two non-human primates, four rodents, three ungulates, opossum, ferret, tree shrew, a bird, a reptile, a teleost fish and a lamprey. We found high molecular conservation of the six retinal cell classes (photoreceptors, horizontal cells, bipolar cells, amacrine cells, retinal ganglion cells (RGCs) and Müller glia), with transcriptomic variation across species related to evolutionary distance. Major subclasses were also conserved, whereas variation among cell types within classes or subclasses was more pronounced. However, an integrative analysis revealed that numerous cell types are shared across species, based on conserved gene expression programmes that are likely to trace back to an early ancestral vertebrate. The degree of variation among cell types increased from the outer retina (photoreceptors) to the inner retina (RGCs), suggesting that evolution acts preferentially to shape the retinal output. Finally, we identified rodent orthologues of midget RGCs, which comprise more than 80% of RGCs in the human retina, subserve high-acuity vision, and were previously believed to be restricted to primates2. By contrast, the mouse orthologues have large receptive fields and comprise around 2% of mouse RGCs. Projections of both primate and mouse orthologous types are overrepresented in the thalamus, which supplies the primary visual cortex. We suggest that midget RGCs are not primate innovations, but are descendants of evolutionarily ancient types that decreased in size and increased in number as primates evolved, thereby facilitating high visual acuity and increased cortical processing of visual information.

Date: 2023
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DOI: 10.1038/s41586-023-06638-9

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