Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype

Author:

Borges Rui12ORCID,Fonseca João1,Gomes Cidália1,Johnson Warren E34,O’Brien Stephen J56,Zhang Guojie789,Gilbert M Thomas P10,Jarvis Erich D1112,Antunes Agostinho12ORCID

Affiliation:

1. CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Portugal

2. Department of Biology, Faculty of Sciences, University of Porto, Portugal

3. Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, Virginia

4. Walter Reed Biosystematics Unit, Smithsonian Institution, Suitland, Maryland

5. Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, Russia

6. Guy Harvey Oceanographic Center, Halmos College of Natural Sciences and Oceanography, Nova Southeastern University

7. Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Denmark

8. China National GeneBank, BGI-Shenzen, Shenzhen, China

9. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

10. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Denmark

11. Laboratory of Neurogenetics of Language, Rockefeller University

12. Howard Hughes Medical Institute, Chevy Chase, Maryland

Abstract

Abstract Typical avian eyes are phenotypically engineered for photopic vision (daylight). In contrast, the highly derived eyes of the barn owl (Tyto alba) are adapted for scotopic vision (dim light). The dramatic modifications distinguishing barn owl eyes from other birds include: 1) shifts in frontal orientation to improve binocularity, 2) rod-dominated retina, and 3) enlarged corneas and lenses. Some of these features parallel mammalian eye patterns, which are hypothesized to have initially evolved in nocturnal environments. Here, we used an integrative approach combining phylogenomics and functional phenotypes of 211 eye-development genes across 48 avian genomes representing most avian orders, including the stem lineage of the scotopic-adapted barn owl. Overall, we identified 25 eye-development genes that coevolved under intensified or relaxed selection in the retina, lens, cornea, and optic nerves of the barn owl. The agtpbp1 gene, which is associated with the survival of photoreceptor populations, was pseudogenized in the barn owl genome. Our results further revealed that barn owl retinal genes responsible for the maintenance, proliferation, and differentiation of photoreceptors experienced an evolutionary relaxation. Signatures of relaxed selection were also observed in the lens and cornea morphology-associated genes, suggesting that adaptive evolution in these structures was essentially structural. Four eye-development genes (ephb1, phactr4, prph2, and rs1) evolved in positive association with the orbit convergence in birds and under relaxed selection in the barn owl lineage, likely contributing to an increased reliance on binocular vision in the barn owl. Moreover, we found evidence of coevolutionary interactions among genes that are expressed in the retina, lens, and optic nerve, suggesting synergetic adaptive events. Our study disentangles the genomic changes governing the binocularity and low-light perception adaptations of barn owls to nocturnal environments while revealing the molecular mechanisms contributing to the shift from the typical avian photopic vision to the more-novel scotopic-adapted eye.

Funder

Russian Science Foundation

St. Petersburg State University

Howard Hughes Medical Institute

Strategic Funding

European Regional Development Fund

National Funds

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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