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 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.
Neurobiology-Neurodegeneration and Repair Laboratory, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA; Department of Life Science, College of Natural Sciences, Chung-Ang University, Seoul 156-756, Republic of Korea.
Jung-Woong
JW
Kim
Neurobiology-Neurodegeneration and Repair Laboratory, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Hyun-Jin
HJ
Yang
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada.
Adam Phillip
AP
Oel
Neurobiology-Neurodegeneration and Repair Laboratory, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Matthew John
MJ
Brooks
Retinal Neurophysiology Section, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Li
L
Jia
Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH 03824, USA.
David Charles
DC
Plachetzki
Retinal Neurophysiology Section, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Wei
W
Li
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada. Electronic address: ted.allison@ualberta.ca.
William Ted
WT
Allison
Neurobiology-Neurodegeneration and Repair Laboratory, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: swaroopa@nei.nih.gov.
Anand
A
Swaroop
D000818:Animals; D050976:Basic-Leucine Zipper Transcription Factors / Q000378:metabolism; D005075:Biological Evolution; D019070:Cell Lineage / Q000235:genetics / Q000528:radiation effects; D002645:Chickens; D002843:Chromatin / Q000378:metabolism; D044127:Epigenesis, Genetic / Q000528:radiation effects; D005136:Eye Proteins / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental / Q000528:radiation effects; D008027:Light; D008322:Mammals / Q000235:genetics / Q000378:metabolism*; D051379:Mice; D055254:Night Vision / Q000528:radiation effects*; D055355:Opsins / Q000378:metabolism; D012045:Regulatory Sequences, Nucleic Acid / Q000235:genetics; D017949:Retinal Cone Photoreceptor Cells / Q000378:metabolism* / Q000528:radiation effects; D017948:Retinal Rod Photoreceptor Cells / Q000378:metabolism* / Q000528:radiation effects; D014466:Ultraviolet Rays; D015027:Zebrafish / Q000196:embryology / Q000378:metabolism
D050976:Basic-Leucine Zipper Transcription Factors; D002843:Chromatin; D005136:Eye Proteins; C084884:Nrl protein, mouse; D055355:Opsins