<p>The Greenland shark (<i>Somniosus microcephalus</i>) is the longest-living vertebrate and inhabits the exceptionally dim and cold waters of the Arctic deep sea. Due to its extreme lifespan, harsh environmental conditions, and prevalent corneal parasitisation, the Greenland shark has previously been thought to have impaired or degenerated vision. Here, we present genomic, transcriptomic, histological and functional evidence that the Greenland shark retains an intact visual system well-adapted for life in dim light. Histology and in vitro opsin expression revealed visual adaptations typical of deep-sea species, including densely packed, elongated rods and a short-wavelength shift in rod visual pigment sensitivity compared to shallow-water sharks. In situ hybridisation confirmed the presence of essential visual cell types: rods, Müller glia, and bipolar, amacrine, and ganglion cells. Moreover, despite being over a century old, the examined specimens showed no obvious signs of retinal degeneration. Using whole genome and retinal RNA-sequencing, we further show that dim-light (rod-based) vision genes are intact and robustly expressed, while many bright-light (cone-based) vision genes have become pseudogenized and/or are no longer expressed. Finally, we identify robust expression of DNA repair-associated genes in the retina, which may help support long-term maintenance of retinal integrity over the Greenland shark’s extreme lifespan.</p>

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The visual system of the longest-living vertebrate, the Greenland shark

  • Lily G. Fogg,
  • Emily Tom,
  • Maxime Policarpo,
  • William Cho,
  • Fangyuan Gao,
  • Doreen Hii,
  • Aaron E. Fawcett,
  • Nicolas Boileau,
  • Amalie Bech-Poulsen,
  • Kirstine F. Steffensen,
  • Cherlyn J. Ng,
  • Peter G. Bushnell,
  • John Fleng Steffensen,
  • Richard Brill,
  • Walter Salzburger,
  • Dorota Skowronska-Krawczyk

摘要

The Greenland shark (Somniosus microcephalus) is the longest-living vertebrate and inhabits the exceptionally dim and cold waters of the Arctic deep sea. Due to its extreme lifespan, harsh environmental conditions, and prevalent corneal parasitisation, the Greenland shark has previously been thought to have impaired or degenerated vision. Here, we present genomic, transcriptomic, histological and functional evidence that the Greenland shark retains an intact visual system well-adapted for life in dim light. Histology and in vitro opsin expression revealed visual adaptations typical of deep-sea species, including densely packed, elongated rods and a short-wavelength shift in rod visual pigment sensitivity compared to shallow-water sharks. In situ hybridisation confirmed the presence of essential visual cell types: rods, Müller glia, and bipolar, amacrine, and ganglion cells. Moreover, despite being over a century old, the examined specimens showed no obvious signs of retinal degeneration. Using whole genome and retinal RNA-sequencing, we further show that dim-light (rod-based) vision genes are intact and robustly expressed, while many bright-light (cone-based) vision genes have become pseudogenized and/or are no longer expressed. Finally, we identify robust expression of DNA repair-associated genes in the retina, which may help support long-term maintenance of retinal integrity over the Greenland shark’s extreme lifespan.