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The energetic cost of vision and the evolution of eyeless Mexican cavefish.

Moran D, Softley R, Warrant EJ - Sci Adv (2015)

Bottom Line: One hypothesis for the reduction of vision in cave animals, such as the eyeless Mexican cavefish, is the high energetic cost of neural tissue and low food availability in subterranean habitats.The cost of vision was calculated to be 15% of resting metabolism for a 1-g fish, decreasing to 5% in an 8.5-g fish as relative eye and brain size declined during growth.Our results demonstrate that the loss of the visual system in the cave phenotype substantially lowered the amount of energy expended on expensive neural tissue during diversification into subterranean rivers, in particular for juvenile fish.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Lund University, Lund 22362, Sweden.

ABSTRACT
One hypothesis for the reduction of vision in cave animals, such as the eyeless Mexican cavefish, is the high energetic cost of neural tissue and low food availability in subterranean habitats. However, data on relative brain and eye mass in this species or on any measure of the energetic cost of neural tissue are not available, making it difficult to evaluate the "expensive tissue hypothesis." We show that the eyes and optic tectum represent significant metabolic costs in the eyed phenotype. The cost of vision was calculated to be 15% of resting metabolism for a 1-g fish, decreasing to 5% in an 8.5-g fish as relative eye and brain size declined during growth. Our results demonstrate that the loss of the visual system in the cave phenotype substantially lowered the amount of energy expended on expensive neural tissue during diversification into subterranean rivers, in particular for juvenile fish.

No MeSH data available.


Related in: MedlinePlus

Output from a model used to calculate the relative energetic costs of eyes, brain, and vision for three Mexican tetra ecotypes.(A) Whole body oxygen consumption (B) relative brain size (C) brain oxygen consumption (D) relative eye size (E) oxygen consumption of eyes (F) oxygen consumption of eyes plus brain (G) oxygen consumption of eyes plus optic tectum. Refer to the Supplementary Materials for the calculative approach.
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Figure 4: Output from a model used to calculate the relative energetic costs of eyes, brain, and vision for three Mexican tetra ecotypes.(A) Whole body oxygen consumption (B) relative brain size (C) brain oxygen consumption (D) relative eye size (E) oxygen consumption of eyes (F) oxygen consumption of eyes plus brain (G) oxygen consumption of eyes plus optic tectum. Refer to the Supplementary Materials for the calculative approach.

Mentions: The oxygen consumption of neural tissue was compared to whole-body oxygen consumption to derive a model of relative neural tissue costs for surface, Micos, and Pachón ecotypes. These costs were modeled for fish body weight ranging from 1 to 8.5 g, the mass range for which relative organ weights were measured and whole-body oxygen consumption data exist (11, 19). Previous research has reported that surface ecotypes have a 19% higher whole-body minimal metabolic rate than Pachón ecotypes (19), whereas Micos ecotypes have an intermediate rate (11) (Fig. 4A). The model predicted that the energetic cost of the whole brain for a 1-g surface fish was 15% of resting metabolism, declining to 5% as relative brain size decreased with body mass (Fig. 4, B and C). Whole-brain energetic costs for Micos and Pachón ecotypes were lower than that for surface ecotypes (reflecting the smaller relative brain size) and decreased from 10 to 6% over the modeled body weight range (Fig. 4C). The energetic cost of eyes in a 1-g surface fish was 8% of resting metabolism, decreasing to 5% in an 8.5-g surface fish (Fig. 4E). The energetic cost of eyes in Micos fish was about 3% over the same mass range (Fig. 4E). The predicted whole-brain energetic costs for larger fish (that is, higher than about 3 g) of the Mexican tetra ecotypes fall in the general range for vertebrates [2 to 8% of resting metabolism (20)]. The cost of neural tissue (that is, eyes plus brain) for a 1-g surface ecotype represented 23% of resting metabolism, whereas for Micos and Pachón ecotypes, the cost was 13 and 10%, respectively (Fig. 4F).


The energetic cost of vision and the evolution of eyeless Mexican cavefish.

Moran D, Softley R, Warrant EJ - Sci Adv (2015)

Output from a model used to calculate the relative energetic costs of eyes, brain, and vision for three Mexican tetra ecotypes.(A) Whole body oxygen consumption (B) relative brain size (C) brain oxygen consumption (D) relative eye size (E) oxygen consumption of eyes (F) oxygen consumption of eyes plus brain (G) oxygen consumption of eyes plus optic tectum. Refer to the Supplementary Materials for the calculative approach.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643782&req=5

Figure 4: Output from a model used to calculate the relative energetic costs of eyes, brain, and vision for three Mexican tetra ecotypes.(A) Whole body oxygen consumption (B) relative brain size (C) brain oxygen consumption (D) relative eye size (E) oxygen consumption of eyes (F) oxygen consumption of eyes plus brain (G) oxygen consumption of eyes plus optic tectum. Refer to the Supplementary Materials for the calculative approach.
Mentions: The oxygen consumption of neural tissue was compared to whole-body oxygen consumption to derive a model of relative neural tissue costs for surface, Micos, and Pachón ecotypes. These costs were modeled for fish body weight ranging from 1 to 8.5 g, the mass range for which relative organ weights were measured and whole-body oxygen consumption data exist (11, 19). Previous research has reported that surface ecotypes have a 19% higher whole-body minimal metabolic rate than Pachón ecotypes (19), whereas Micos ecotypes have an intermediate rate (11) (Fig. 4A). The model predicted that the energetic cost of the whole brain for a 1-g surface fish was 15% of resting metabolism, declining to 5% as relative brain size decreased with body mass (Fig. 4, B and C). Whole-brain energetic costs for Micos and Pachón ecotypes were lower than that for surface ecotypes (reflecting the smaller relative brain size) and decreased from 10 to 6% over the modeled body weight range (Fig. 4C). The energetic cost of eyes in a 1-g surface fish was 8% of resting metabolism, decreasing to 5% in an 8.5-g surface fish (Fig. 4E). The energetic cost of eyes in Micos fish was about 3% over the same mass range (Fig. 4E). The predicted whole-brain energetic costs for larger fish (that is, higher than about 3 g) of the Mexican tetra ecotypes fall in the general range for vertebrates [2 to 8% of resting metabolism (20)]. The cost of neural tissue (that is, eyes plus brain) for a 1-g surface ecotype represented 23% of resting metabolism, whereas for Micos and Pachón ecotypes, the cost was 13 and 10%, respectively (Fig. 4F).

Bottom Line: One hypothesis for the reduction of vision in cave animals, such as the eyeless Mexican cavefish, is the high energetic cost of neural tissue and low food availability in subterranean habitats.The cost of vision was calculated to be 15% of resting metabolism for a 1-g fish, decreasing to 5% in an 8.5-g fish as relative eye and brain size declined during growth.Our results demonstrate that the loss of the visual system in the cave phenotype substantially lowered the amount of energy expended on expensive neural tissue during diversification into subterranean rivers, in particular for juvenile fish.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Lund University, Lund 22362, Sweden.

ABSTRACT
One hypothesis for the reduction of vision in cave animals, such as the eyeless Mexican cavefish, is the high energetic cost of neural tissue and low food availability in subterranean habitats. However, data on relative brain and eye mass in this species or on any measure of the energetic cost of neural tissue are not available, making it difficult to evaluate the "expensive tissue hypothesis." We show that the eyes and optic tectum represent significant metabolic costs in the eyed phenotype. The cost of vision was calculated to be 15% of resting metabolism for a 1-g fish, decreasing to 5% in an 8.5-g fish as relative eye and brain size declined during growth. Our results demonstrate that the loss of the visual system in the cave phenotype substantially lowered the amount of energy expended on expensive neural tissue during diversification into subterranean rivers, in particular for juvenile fish.

No MeSH data available.


Related in: MedlinePlus