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

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 retinae. 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. Overall design: GFP positive cells from Nrlp-GFP mouse retinas at post-natal ages P2, P10, and P28 were isolated by flow sorting by FACSAria II (Becton Dickinson). DNA was extracted by Purelink gDNA isolation kit (Life technologies). Reduced Representation Bisulfite Sequencing library construction using 50 ng of DNA as input. Libraries were constructed using a modification of the Illumina TruSeq DNA. Bisulfite modification was performed using Epitech kit (Qiagen). Each library was single-end sequenced in an independent lane of a GAIIx at a length of 76 bases. Fastq files were generated from reads passing chastity filter.