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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

Summary graphs of respirometry data showing the oxygen consumption rates of eyes and brains in surface and Pachón ecotypes at different times of day.Each gray line represents a single organ measurement. A running mean ± 95% confidence interval is overlaid.
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Figure 3: Summary graphs of respirometry data showing the oxygen consumption rates of eyes and brains in surface and Pachón ecotypes at different times of day.Each gray line represents a single organ measurement. A running mean ± 95% confidence interval is overlaid.

Mentions: We measured the energy demand of the whole brain of Pachón fish and the energy demand of the whole brain and eyes of surface fish using isolated organ oxygen consumption measurements. Whole eyes and brains were dissected out from 10 Pachón and 10 surface ecotypes and placed inside individual respirometry chambers supplied with artificial cerebrospinal fluid. The cerebrospinal fluid was replaced every 10 min, allowing for repeated oxygen consumption measurements to be made over a 24-hour period. In total, we performed 1568 determinations of oxygen consumption from 18 eyes (n = 39 to 97 for a single eye) and 1736 determinations of whole-brain oxygen consumption from 10 surface ecotypes and 10 Pachón ecotypes (n = 66 to 96 for a single brain) (Fig. 3). Mass-specific brain oxygen consumption rates did not differ between ecotypes (F1,18 = 1.43, P = 0.23). The effects of light and dark exposure on eye oxygen consumption were evaluated using nested analysis of variance (light-dark nested in individual organs). The oxygen consumption of eyes was significantly higher (F1,18 = 4.64, P = 0.000) in the dark (mean ± SD, 0.542 ± 0.405 mg O2 hour−1 g wet mass−1) than in the light (mean ± SD, 0.507 ± 0.260 mg O2 hour−1 g wet mass−1); however, the effect size of this variable was small (∂η2 = 0.052) and considerably less than the effect size of the variation between individual eyes (∂η2 = 0.304). Therefore, we decided to ignore light as a variable for modeling purposes, and a single mean oxygen consumption rate was calculated for all eye data (mean ± SD, 0.525 ± 0.342 mg O2 hour−1 g wet mass−1). The mean whole-eye (sclera plus retina minus lens and vitreous) respiration rate (0.525 mg O2 hour−1 g wet tissue−1) was broadly similar to the only other metabolic rate measurement made of a fish retina [retinal tissue of the rainbow trout Oncorhynchus mykiss, 1.498 mg O2 hour−1 g wet tissue−1 (15)], taking into account that an isolated retina contains considerably more metabolically active tissue compared to a retina mounted on a sclera [the latter is largely composed of connective tissue (16) with minimal metabolic activity]. Mass-specific brain oxygen consumption rates did not differ between surface ecotypes and Pachón ecotypes (F1,18 = 1.43, P = 0.232), and the mean brain respiration rate for all experiments (1.603 mg O2 hour−1 g wet tissue−1) fell in the range reported for other fish [0.72 to 2.02 mg O2 hour−1 g wet tissue−1 (17, 18)].


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

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

Summary graphs of respirometry data showing the oxygen consumption rates of eyes and brains in surface and Pachón ecotypes at different times of day.Each gray line represents a single organ measurement. A running mean ± 95% confidence interval is overlaid.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Summary graphs of respirometry data showing the oxygen consumption rates of eyes and brains in surface and Pachón ecotypes at different times of day.Each gray line represents a single organ measurement. A running mean ± 95% confidence interval is overlaid.
Mentions: We measured the energy demand of the whole brain of Pachón fish and the energy demand of the whole brain and eyes of surface fish using isolated organ oxygen consumption measurements. Whole eyes and brains were dissected out from 10 Pachón and 10 surface ecotypes and placed inside individual respirometry chambers supplied with artificial cerebrospinal fluid. The cerebrospinal fluid was replaced every 10 min, allowing for repeated oxygen consumption measurements to be made over a 24-hour period. In total, we performed 1568 determinations of oxygen consumption from 18 eyes (n = 39 to 97 for a single eye) and 1736 determinations of whole-brain oxygen consumption from 10 surface ecotypes and 10 Pachón ecotypes (n = 66 to 96 for a single brain) (Fig. 3). Mass-specific brain oxygen consumption rates did not differ between ecotypes (F1,18 = 1.43, P = 0.23). The effects of light and dark exposure on eye oxygen consumption were evaluated using nested analysis of variance (light-dark nested in individual organs). The oxygen consumption of eyes was significantly higher (F1,18 = 4.64, P = 0.000) in the dark (mean ± SD, 0.542 ± 0.405 mg O2 hour−1 g wet mass−1) than in the light (mean ± SD, 0.507 ± 0.260 mg O2 hour−1 g wet mass−1); however, the effect size of this variable was small (∂η2 = 0.052) and considerably less than the effect size of the variation between individual eyes (∂η2 = 0.304). Therefore, we decided to ignore light as a variable for modeling purposes, and a single mean oxygen consumption rate was calculated for all eye data (mean ± SD, 0.525 ± 0.342 mg O2 hour−1 g wet mass−1). The mean whole-eye (sclera plus retina minus lens and vitreous) respiration rate (0.525 mg O2 hour−1 g wet tissue−1) was broadly similar to the only other metabolic rate measurement made of a fish retina [retinal tissue of the rainbow trout Oncorhynchus mykiss, 1.498 mg O2 hour−1 g wet tissue−1 (15)], taking into account that an isolated retina contains considerably more metabolically active tissue compared to a retina mounted on a sclera [the latter is largely composed of connective tissue (16) with minimal metabolic activity]. Mass-specific brain oxygen consumption rates did not differ between surface ecotypes and Pachón ecotypes (F1,18 = 1.43, P = 0.232), and the mean brain respiration rate for all experiments (1.603 mg O2 hour−1 g wet tissue−1) fell in the range reported for other fish [0.72 to 2.02 mg O2 hour−1 g wet tissue−1 (17, 18)].

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