Retinal oxygen supply shaped the functional evolution of the vertebrate eye

Author:

Damsgaard Christian12ORCID,Lauridsen Henrik34,Funder Anette MD5,Thomsen Jesper S6,Desvignes Thomas7,Crossley Dane A8,Møller Peter R9,Huong Do TT10,Phuong Nguyen T10,Detrich H William11ORCID,Brüel Annemarie6,Wilkens Horst12,Warrant Eric13,Wang Tobias1,Nyengaard Jens R14,Berenbrink Michael15,Bayley Mark1

Affiliation:

1. Section for Zoophysiology, Department of Bioscience, Aarhus University, Aarhus, Denmark

2. Department of Zoology, University of British Columbia, Vancouver, Canada

3. Department of Clinical Medicine, Aarhus University, Aarhus, Denmark

4. Meinig School of Biomedical Engineering, Cornell University, Ithaca, United States

5. Department of Forensic Medicine, Aarhus University, Aarhus, Denmark

6. Department of Biomedicine, Aarhus University, Aarhus, Denmark

7. Institute of Neuroscience, University of Oregon, Eugene, United States

8. Department of Biological Sciences, University of North Texas, Denton, United States

9. Section for Evolutionary Genomics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

10. College of Aquaculture and Fisheries, Can Tho University, Can Tho, Viet Nam

11. Department of Marine and Environmental Sciences, Marine Science Center, Northeastern University, Nahant, United States

12. Zoological Institute and Zoological Museum, University of Hamburg, Hamburg, Germany

13. Department of Biology, Lund University, Lund, Sweden

14. 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

15. Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom

Abstract

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.

Funder

Danida Fellowship Centre

Carlsbergfondet

Biotechnology and Biological Sciences Research Council

Danish Council for Independent Research

National Science Foundation

Villum Fonden

Velux Fonden

Karen Elise Jensens Fond

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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2. Metabolic Relationships Between the Retina and Retinal Pigmented Epithelium;Reference Module in Neuroscience and Biobehavioral Psychology;2024

3. Visual opsin gene expression evolution in the adaptive radiation of cichlid fishes of Lake Tanganyika;Science Advances;2023-09-08

4. Conservatism and Variability of the Antioxidant Defense System in the Retinal Pigment Epithelium of Vertebrates;Journal of Evolutionary Biochemistry and Physiology;2023-05

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