Section for Zoophysiology, Department of Bioscience, Aarhus University, Aarhus, Denmark; Department of Zoology, University of British Columbia, Vancouver, Canada
Henrik Lauridsen
Department of Clinical Medicine, Aarhus University, Aarhus, Denmark; Meinig School of Biomedical Engineering, Cornell University, Ithaca, United States
Anette MD Funder
Department of Forensic Medicine, Aarhus University, Aarhus, Denmark
Jesper S Thomsen
Department of Biomedicine, Aarhus University, Aarhus, Denmark
Thomas Desvignes
Institute of Neuroscience, University of Oregon, Eugene, United States
Dane A Crossley II
Department of Biological Sciences, University of North Texas, Denton, United States
Peter R Møller
Section for Evolutionary Genomics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
Do TT Huong
College of Aquaculture and Fisheries, Can Tho University, Can Tho, Viet Nam
Nguyen T Phuong
College of Aquaculture and Fisheries, Can Tho University, Can Tho, Viet Nam
Department of Marine and Environmental Sciences, Marine Science Center, Northeastern University, Nahant, United States
Annemarie Brüel
Department of Biomedicine, Aarhus University, Aarhus, Denmark
Horst Wilkens
Zoological Institute and Zoological Museum, University of Hamburg, Hamburg, Germany
Eric Warrant
Department of Biology, Lund University, Lund, Sweden
Tobias Wang
Section for Zoophysiology, Department of Bioscience, Aarhus University, Aarhus, Denmark
Jens R Nyengaard
Core Center for Molecular Morphology, Section for Stereology and Microscopy, Centre for Stochastic Geometry and Advanced Bioimaging, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
Michael Berenbrink
Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
Mark Bayley
Section for Zoophysiology, Department of Bioscience, Aarhus University, Aarhus, Denmark
The retina has a very high energy demand but lacks an internal blood supply in most vertebrates. Here we explore the hypothesis that oxygen diffusion limited the evolution of retinal morphology by reconstructing the evolution of retinal thickness and the various mechanisms for retinal oxygen supply, including capillarization and acid-induced haemoglobin oxygen unloading. We show that a common ancestor of bony fishes likely had a thin retina without additional retinal oxygen supply mechanisms and that three different types of retinal capillaries were gained and lost independently multiple times during the radiation of vertebrates, and that these were invariably associated with parallel changes in retinal thickness. Since retinal thickness confers multiple advantages to vision, we propose that insufficient retinal oxygen supply constrained the functional evolution of the eye in early vertebrates, and that recurrent origins of additional retinal oxygen supply mechanisms facilitated the phenotypic evolution of improved functional eye morphology.
