Retinal oxygen supply shaped the functional evolution of the vertebrate eye

TY - JOUR

T1 - Retinal oxygen supply shaped the functional evolution of the vertebrate eye

AU - Damsgaard, Christian

AU - Lauridsen, Henrik

AU - Funder, Anette Marianne Daa

AU - Thomsen, Jesper Skovhus

AU - Desvignes, Thomas

AU - Crossley, II, Dane A.

AU - Møller, Peter Rask

AU - Huong, Do Thi Thanh

AU - Phuong, Nguyen T.

AU - Detrich, H William

AU - Brüel, Annemarie

AU - Wilkens, Horts

AU - Warrant, Eric

AU - Wang, Tobias

AU - Nyengaard, Jens Randel

AU - Berenbrink, Michael

AU - Bayley, Mark

PY - 2019/12

Y1 - 2019/12

N2 - 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.

AB - 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.

U2 - 10.7554/eLife.52153

DO - 10.7554/eLife.52153

M3 - Journal article

C2 - 31820735

SN - 2050-084X

VL - 8

JO - eLife

JF - eLife

M1 - e52153

ER -