At some point back in deep time, a group of fish were washed into a limestone cave somewhere in northeastern Mexico. With no way out and little more than bat droppings to eat, the fish began to adapt to their new troglodytic lifestyle. Unable to see other members of their group in the dark, they lost their colourful pigmentation. Then they lost their eyesight, their eyes gradually got smaller, and then disappeared altogether.

This was accompanied by a dramatic reduction in the size of the brain’s visual system. Yet, the question of why the blind cave fish lost its eyes and a large part of its brain remains unresolved. Now, biologists in Sweden believe they have found the answer. In new research published today, they report that loss of the visual system saves the fish a substantial amount of energy, and was probably key to their stranded ancestors’ survival.

The blind cave fish Astyanax mexicanus is adapted to its subterranean environment in other ways. As its vision regressed, it became more reliant on smell and taste, and its taste buds grew larger and more numerous. They also developed an enhanced ability to detect changes in mechanical pressure, which made them more sensitive to water movements.

Last year, Damian Moran of Lund University and his colleagues reported that blind cave fish eliminated the circadian rhythm in their metabolism during their course of evolution, and that this leads to a massive 27% reduction in their energy expenditure. This new study was designed test whether or not they lost their visual system for the same reason.

Darwin found it hard to imagine why eyes might be harmful to animals living in perpetual darkness, and attributed their loss “solely to disuse.” According to another hypothesis, however, the reduction of vision occurred because growing and maintaining eyes and brain tissue requires huge amounts of energy.

The human brain perfectly illustrates just how energetically costly brain tissue is. It consumes one quarter of the body’s energy, despite making up just 2% of body mass, and nearly one third of the cerebral cortex is devoted to processing visual information.

It’s hard finding convincing evidence for this ‘expensive tissue hypothesis,’ however, mostly because it’s usually impossible to compare the rate of energy consumption in a living organism with that of its ancient evolutionary ancestor. But blind cave fish are ideal for testing the idea, because their ancestors – the surface-dwelling form – still inhabit the rivers of northeastern Mexico and Texas.

Moran and his colleagues therefore collected specimens of blind cave fish, their surface-dwelling counterparts, plus a hybrid form with some pigmentation and eye remnants, from caves and rivers in Mexico, and took them back to the lab in Sweden, where they used specially-built respirometry apparatus to measure and compare the size and metabolic rates of the fish and all their internal organs.

Their results, published in the journal Science Advances, show that although the heart, digestive system, and gonads were roughly the same size and weight in all three, and used roughly the same amounts of energy, the gills of the cave-dwelling form were much larger than those of the other two, enabling them breathe in the oxygen-deprived cave environment.

The brains of surface-dwelling fish were also roughly 30% larger than those of the blind cave fish, while those of the hybrids were of intermediate size. In the surface-dwellers, brain size increases relative to body mass, such that bigger individuals have larger brains. In the cave-dwellers, however, no such relationship exists – all had significantly smaller brains, due to significant reduction in the size of a midbrain region called the optic tectum, which normally receives visual inputs from the eyes.

These size reductions significantly reduced energy costs. The researchers calculated the energy cost of the brain to be about 15% of the resting metabolic rate for a surface-dwelling fish weighing 1g, decreasing to 5% in 8.5g fish, compared to 4% and 3% for hybrids of those respective size and mass. And the eyes consume about 8% of resting metabolism in surface-dwellers weighing 8.5g, decreasing to 5% in the largest specimens.

Overall, the brain accounts for some 23% of the resting metabolic rate in the surface-dwellers, compared to just 10% in the blind cave fish. Thus, the reduced size of the visual parts of the brain lowers total energy consumption by about 30% compared to surface-dwelling fish.

This is strong evidence that cave-dwelling organisms lost their visual systems in order to save energy. The findings also provide insights into how different types of evolutionary pressure can drive brain evolution.

According to another hypothesis, the invention of cooking was a major driving force for evolution of the human brain, because it would have released more energy from the food that our ancestors ate, allowing the brain to expand and the gut to shrink. It seems that the opposite happened to the ancestors of the blind cave fish – finding themselves trapped in that dark cave, their brains shrank dramatically, in order to save energy and ensure their survival.

Reference

Moran, D., et al. (2015). The energetic cost of vision and the evolution of eyeless Mexican cavefish. Sci. Adv.,1:e1500363 [Abstract]