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

Dev Cell. 2016 Jun 20;37(6):520-32. doi: 10.1016/j.devcel.2016.05.023.

Abstract

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.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic-Leucine Zipper Transcription Factors / metabolism
  • Biological Evolution*
  • Cell Lineage / genetics
  • Cell Lineage / radiation effects
  • Chickens
  • Chromatin / metabolism
  • 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

Substances

  • Basic-Leucine Zipper Transcription Factors
  • Chromatin
  • Eye Proteins
  • Nrl protein, mouse
  • Opsins