Recruitment of Rod Photoreceptors from Short-Wavelength-Sensitive Cones during the Evolution of Nocturnal Vision in Mammals

• Published in: Developmental cell Vol. 37; no. 6; pp. 520 - 532
• Main Authors: Kim, Jung-Woong, Yang, Hyun-Jin, Oel, Adam Phillip, Brooks, Matthew John, Jia, Li, Plachetzki, David Charles, Li, Wei, Allison, William Ted, Swaroop, Anand
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 20.06.2016
• Subjects: Animals; Basic-Leucine Zipper Transcription Factors - metabolism; Biological Evolution; Cell Lineage - genetics; Cell Lineage - radiation effects; Chickens; Chromatin - metabolism; Danio rerio; Epigenesis, Genetic - radiation effects; Eye Proteins - metabolism; Gene Expression Regulation, Developmental - radiation effects; Light; Mammals - genetics; Mammals - metabolism; Mice; Night Vision - radiation effects; Opsins - metabolism; Regulatory Sequences, Nucleic Acid - genetics; Retinal Cone Photoreceptor Cells - metabolism; Retinal Cone Photoreceptor Cells - radiation effects; Retinal Rod Photoreceptor Cells - metabolism; Retinal Rod Photoreceptor Cells - radiation effects; Ultraviolet Rays; Zebrafish - embryology; Zebrafish - metabolism
• ISSN: 1534-5807; 1878-1551; 1878-1551
• DOI: 10.1016/j.devcel.2016.05.023

Vertebrate ancestors had only cone-like photoreceptors. The duplex retina evolved in jawless vertebrates with the advent of highly photosensitive rod-like photoreceptors. Despite cones being the arbiters of high-resolution color vision, rods emerged as the dominant photoreceptor in mammals during a nocturnal phase early in their evolution. We investigated the evolutionary and developmental origins of rods in two divergent vertebrate retinas. In mice, we discovered genetic and epigenetic vestiges of short-wavelength cones in developing rods, and cell-lineage tracing validated the genesis of rods from S cones. Curiously, rods did not derive from S cones in zebrafish. Our study illuminates several questions regarding the evolution of duplex retina and supports the hypothesis that, in mammals, the S-cone lineage was recruited via the Maf-family transcription factor NRL to augment rod photoreceptors. We propose that this developmental mechanism allowed the adaptive exploitation of scotopic niches during the nocturnal bottleneck early in mammalian evolution. [Display omitted] •Rod photoreceptors in mouse retina show genetic and epigenetic vestiges of S cones•Rod photoreceptors in mice but not zebrafish exhibit S-cone lineage•NRL locus of early mammals accrued regulatory elements driving rod-dominant retina•Recruitment of S cones to rods in mammals helped mitigate the nocturnal bottleneck The evolution of rod-dominant retinas was a critical adaptation, allowing mammalian ancestors to survive a nocturnal bottleneck. Kim et al. provide evidence suggesting that this evolutionary transition was driven by molecular innovations in the Maf-family protein NRL, which led to the recruitment of rods from S cones in early mammals.