Some 300m below the ocean surface it is always twilight, and cold…  The water is barely above zero.  Fast-moving squid hide here from predatory fish which stay near the surface; at this depth, their nerves would be so slowed by the cold that their eyes could no longer see for them to hunt effectively.

But there are exceptions; a stealthy predator dives into this semi darkness.  Whilst the swordfish’s body temperature matches that of the water, its eyes and brain, crucially, stay toasty warm at around 23⁰C.

---

Why do swordfish have warm eyes?

A fish’s body temperature usually matches that of the water, meaning they are ‘cold blooded’ (poikilothermic).  Swordfish nerves, like ours and those of other vertebrates, operate only within narrow temperature limits.  The squid is also ‘cold-blooded’, but their elongated nerve cell axons however, are unusually wide, around 0.5mm diameter, and operate well in the cold, allowing them to maintain their fast movements and escape predators.

A few fish species, however, have evolved methods to generate heat in some of their tissues.  Under the chilly, low light conditions of the deep sea, the warm eyes of the swordfish keep its optical nerve signals rapid.  This allows it to register more visual signals per second than can other vertebrate predators.  This fast image resolution ‘slows down’ apparent time and amplifies details, allowing these stealthy hunters to discern the brief flashes of silver that reveal the fleeting movements of small fish and squid.

This prompts some key evolutionary questions;

– How is the swordfish’s eye heat generated?

– How does the swordfish keep the heat localised to its eyes and brain?

– How does keeping body parts at different temperatures adapt swordfish for survival?

How is the swordfish’s eye heat generated?

Swordfish eye muscles contain many brown-coloured cells that produce heat without shivering (non-shivering thermogenesis).  They have a high metabolism (respiration rate) and contain many of the organelles known as mitochondria.

Mitochondria are formerly free-living bacteria found inside nearly all animal, plant and fungal cells. They ‘breathe’ for their cell, converting sugars and oxygen into carbon dioxide and water.  This releases energy, which they use to pump hydrogen ions (H⁺, protons) from the internal matrix into their inter-membrane space.  They use the chemical energy gradient this creates to produce adenosine triphosphate (ATP), life’s energy storage compound.  These cellular energy factories are found in all animals and plants.

Humans and other mammals have brown adipose cells, also called ‘brown fat’.  The mitochondria in these cells make very little ATP.  Instead, ‘uncoupling proteins’ rearrange negatively charged fatty acids in the mitochondrial inner membranes to face into the inter-membrane space.  These associate with the positively charged protons, then ‘flip-flop’, carrying them back into the matrix and dissipating the energy gradient as heat.

How does the swordfish keep the heat localised to its eyes and brain?

When our bodies generate heat in a cold environment, this sets up an energy gradient; the bigger the differences between our internal and external temperature, the faster we cool.  Warm bodies in a cold environment lose heat quickly, unless insulated.  Birds use feathers, most mammals use fur and whales have blubber.

Fatty insulation over the swordfish’s skull retains heat, and helps keep its eyes and brain at a near constant temperature.  These tissues are homeothermic (maintaining a stable temperature), whilst the rest of its body is poikilothermic (allowing temperatures to vary with the environment).  Blood vessels supplying oxygen to the swordfish’s eye muscles are also arranged to retain heat.  These vessels run in parallel, allowing outgoing veins to warm incoming arteries (this is known as a ‘counter-current’ heat exchange system).

Insulation (fur, feathers or fat), combined with a blood supply arranged to allow counter-current heat exchange, are found in many cold-adapted animals.  Lowering surface temperatures reduces the energy difference between a body and its surroundings, so minimising heat loss.  Warm-bodied migrating species such as wolves and many birds from polar regions use a counter-current exchange to reduce the temperatures of their legs and feet.  This means that their body parts in contact with snow or ice remain at just above zero.

How does keeping body parts at different temperatures adapt swordfish for survival? 

Keeping your body at a different temperature from your environment requires a lot of energy.  The swordfish’s ‘dual temperature’ body isolates the heat and keeps it in one well-insulated region; this is the most energy efficient way for these ‘wait and sprint’ hunters to survive in this environment.  Tuna are another example of a fish with warm and cool tissues.  Their red muscles along their spine are warm, and sustain constant ‘slow’ strokes of the tail during their long distance migrations.

When we sweat, water evaporates and cools our skin surfaces.  Dogs and many other mammals pant to evaporate water from their tongue and mouth cavity.  Elephants lack both sweat glands and a panting reflex; these are possible remnants of their aquatic ancestry.

In very high temperatures they enter a whole-body heterothermic state.  They slow their metabolism, lowering their morning body temperature.  They then absorb daytime heat, raising their temperature above 36.7⁰C, and radiate this ‘stored’ heat at night.

Varying the temperature at times like elephants, or in certain tissues like swordfish, is known as heterothermy.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Carey, F.G. (1982)  A brain heater in the swordfish.  Science 216, 1327-1329.

Fritsches, K.A. et al. (2005)  Warm eyes provide superior vision in swordfishes.  Current Biology 15, 55-58.

Guderley, H. et al. (2005)  Why are some mitochondria more powerful than others; insights from comparisons of muscle mitochondria from three terrestrial vertebrates.  Comparative Biochemistry and Physiology, B 142, 172-180.

Hulbert, A.J. et al. (2006)  How might you compare mitochondria from different tissues and different species?  Journal of Comparative Physiology, B 176, 93-105.

Kowaltowski, A.J. (2000)  Alternative mitochondrial functions in cell physiopathology; beyond ATP production.  Brazilian Journal of Medical and Biological Research 33, 241-250.

Nespolo, R.F. et al. (2011)  Using new tools to solve an old problem; the evolution of endothermy in vertebrates.  Trends in Ecology and Evolution 26, 414-423.

Warrand, E.J. and Locket, N.A. (2004)  Vision in the deep sea.  Biological Reviews 79, 671-712.

Weissenbrock, N.M. et al. (2012)  Taking the heat; thermoregulation in Asian elephants under different climatic conditions.  Journal of Comparative Physiology, B 182, 311-319.

As the bats chatter above you in the cavern roof, their droppings rain down into the pool below.  The floor is silky with bacteria.  It’s cold and still.  A musty tang lingers in the air.  

You are completely blind.  You rely on hairs in your skin to feel for movement in the water. 

You are hungry.  Something is disturbing the mud; you can smell it!   You follow the scent trail and grab at it.  It feels like a shrimp. 

Things touch and nip you…  You are afraid of being eaten.  You move slowly, dozing for short periods, but don’t sleep. 

You have been here for…  How long?  Can you tell this without a sense of day and night?

---

Mexico’s blind cave fish show many of the adaptations found in animals from cave ecosystems across the world.  They have lost their eyes, and instead have chemoreceptors (‘taste buds’) scattered over their skin, allowing them to follow ‘pathways’ of chemical concentration (chemotaxis).  Touch-sensitive hairs around the mouth, along with a well-developed lateral line system, enable them to sense tiny water currents caused by prey and other fish.

In these caves, as in the deep sea, food is always in short supply.  To avoid being eaten by other fish they must remain vigilant, and so may ‘doze’ but do not sleep.  These fish have a low metabolic rate to conserve energy, and build up reserves of body fat .

Why do these fish and other cave dwellers go blind? One explanation is that eye loss is neutral to their survival.  When a characteristic is no longer essential to survival, mutations (mistakes in the DNA) that cause crucial genes to cease working are not selected against.  They are then passed to the next generation ‘at random’.

These small populations of cave fish were likely founded from only a few individuals.  We could anticipate that neutral mutations present in these founders would become widespread in the population by chance.  However these cave fish have evolved separately multiple times.  If the loss of eyes and skin pigment were a random, neutral process, we could expect some of these populations to have retained their sight and colour.  Also the PAX6 gene, used to build eyes in nearly all animals, is present and working in these fish.

Another possibility is energy conservation.  Eyes are costly to build and maintain, so disposing of them in this energy-poor environment seems a sensible option.  This however doesn’t fit the facts.  Eye cups are present in day-old embryos.  By day two, the lens cells are beginning to grow and divide, but in these cave fish a process of deliberate ‘cell death’ destroys them as they arise.  This strategy seems neither neutral nor particularly economic.

So what is really driving the evolution of these pale, sightless and sleepless fish?  Genetic studies are providing some alternative answers that shine light into how evolution really works.

Why do cave fish kill off their own eyes? 

The PAX gene plays a key role in the development of eyes in vertebrate embryos.  PAX6 action is reduced by increases in the activity of another gene, called HEDGEHOG whichdefines boundaries between cell types and promotes development of the fish’s lateral line, jaws, teeth and taste buds.  HEDGEHOG is more active in cave fish embryos than in their sighted sister species, causing the lateral line cell zone and the jaw to expand.  As it does so, this also switches off PAX6 and halts eye development.

This trade-off between ‘touch and taste’ versus ‘sight’ enhances the very senses that the cave fish needs in its ever-dark world.  Eye shrinkage, which reduces the energy budget, is a secondary effect of selection for these other senses.  This subtle change in the key interaction of two developmental genes  at a critical stage can radically alter a gene’s effect and the body which results.

What does enhanced touch sensitivity provide for these fish?

Try stroking your eyebrow against the direction of hair growth. Now stroke your forehead. Which feels like a stronger movement?

Hairs in our skin enable us to be more sensitive to touch.  The Mexican blind cave fish have a lateral line systemlike all fish.  All lateral line systems use tiny hair cells to detect changes in water movement, but in these cave dwellers it is unusually sensitive.

These fish also have a behaviour which seems counter-intuitive.  If introduced into a new environment, instead of slowing down and moving cautiously, they swim faster.  The reason is that more rapid movements increase the flow of information to the hair cells.  This expands their awareness, providing a larger ‘hydrodynamic image’ of their world.  Also at greater speeds, the water layer that clings to their skin is reduced, helping to make this image ‘sharper’.

Why are cave fish so pale?

The melanin-based pigments in our skin and those of other animals provide colour and pattern, but they have a more ancient evolutionary role: to  protect us from damage by ultraviolet light.  Without sunlight, cave animals typically are colourless.  In Mexican cave fish this is connected to a loss-of-function mutation (in the gene oca2), controlling the first step of pigment production.

Independently evolved populations of cave fish are colourless thanks to unique mutations in this same gene.  This is curious.  If pigment loss occurred by chance, we would expect that some populations would have shut down later stages of pigment production, as this would give the same effect.  This specific mutation suggests instead that pigment loss has been actively selected.

Pigment loss may conserve energy, and it is possible that mutating the genes controlling later biosynthetic stages may have other effects that reduce fitness.  However a more compelling explanation is that shutting down oca2 increases the availability of tyrosine, an amino acid.  What is so special about tyrosine?

Neurotransmitter production depends upon the tyrosine supply.  The fish produces the neurotransmitters dopamine and noradrenaline (norepinephrine), and the hormone adrenaline (epinephrine), from tyrosine.  Cavefish brains have higher concentrations of these chemicals than brains of sighted fish.  Noradrenaline and adrenaline provoke the ‘fight or flight response; in these fish they are linked to the minimal amounts of sleep and the ability to engage in unusually fast foraging.

Adaptation to life in caves has produced a range of animals with some remarkably similar characteristics.  It seems that Mexico’s cave fish have made an evolutionary trade-off.  Faster swimming and an enhanced sensitivity to touch and taste comes at the cost of eyes and skin colour.  And it keeps them awake in the dark.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Bibliowicz, J, et al. (2013)  Differences in chemosensory response between eyed and eyeless Astyanax mexicanus of the Rio Subterráneo cave.  EvoDevo 4, e25.

Bilanžija, H. et al. (2013)  A potential benefit of albinism in Astyanax cave fish: down-regulation of the oca2 gene increases tyrosine and catecholamine levels as an alternative to melanin synthesis.  PLoS ONE 8, e80823.

Burt de Perera, T. and Braithwaite, V.A.  (2005)  Laterality in a non-visual sensory modality — the lateral line of fish.  Current Biology 15, R241-R242.

Coombs, S. et al. (2000)  Hydrodynamic image formation by the peripheral lateral line system of the Lake Michigan mottled sculpin, Cottus bairdi.  Philosophical Transactions of the Royal Society of London, B 355, 1111-1114.

Ćurčić-Blake, B. and van Netten, S.M. (2006)  Source location encoding in the fish lateral line canal.  Journal of Experimental Biology 209, 1548-1559.

Horstkotte, J. et al. (2010)  Predation by three species of spiders on a cavefish (Poecilia mexicana, Poeciliidae) in a Mexican sulphur cave.  Bulletin of the British Arachnological Society 15, 55-58.

Jeffery, W.R. (2001)  Cavefish as a model system in evolutionary developmental biology.  Developmental Biology 231, 1–12.

Jeffery, W.R. (2009)  Regressive evolution in Astyanax cave fish.  Annual Review of Genetics 43, 25-47.

Jeffery, W.R. et al. (2003)  To see or not to see: evolution of eye development in Mexican Blind Cavefish.  Integrative Comparative Biology 43, 531–541.

Mueller, K.P. et al. (2014)  Sunscreen for fish: the co-option of UV light protection for camouflage.  PLoS ONE 9, e87372.

Niven, J.E. (2008)  Evolution: convergent eye losses in fishy circumstances.  Current Biology 18, R27–R29.

Rétaux, S. and Casane, D. (2013)  Evolution of eye development in the darkness of caves: adaptation, drift, or both?  EvoDevo 4, 26.

Sanford, W.E. et al. (2006)  Research Opportunities in Interdisciplinary Ground-Water Science in the U.S. Geological Survey.  Circular 1293. U.S. Geological Survey.

Strickler, A.G. et al. (2007)  The lens controls cell survival in the retina: evidence from the blind cavefish Astyanax. Developmental Biology 311, 512-523.

Tian, N.M. and Price, D.J. (2005)  Why cavefish are blind. BioEssays 27, 235-238.

Wilkens, H. and Strecker, U. (2003)  Convergent evolution of the cavefish Astyanax (Characidae, Teleostiei): genetic evidence from reduced eye-size and pigmentation.  Biological Journal of the Linnean Society 80, 545–554.

Wilkens, H. (1988)  Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces).  Evolutionary Biology 23, 271–367.

Yamamoto, Y. et al. (2004)  Hedgehog signalling controls eye degeneration in blind cavefish.  Nature 431, 844-847.