Tuesday, 19 May 2015

Why I'm excited about the opah

Last week, a new paper in Science (Wegner et al. 2015) announced that they had discovered whole body endothermy (that is, the ability to generate metabolic heat to keep the temperature of the internal organs above ambient temperature) in a pelagic bony fish. This fact is intrinsically cool, but as a mammalian paleontologist who is interested in the evolution of mammalian physiology, I was immediately intrigued and excited to know more.
Everyone knows that mammals and birds are "warm blooded", that is that they maintain a stable body temperature that is above that of the environment. Usually, they are described this way to distinguish them from lizards, snakes, crocodiles, amphibians and fish, collectively referred to as "cold blooded". But the details of heat physiology are much more complex than this simplistic dichotomy. At the most fundamental level, there are two different, and related axes of variation along which animals can be placed to describe their body temperature physiology.
One axis separates animals that maintain a constant body temperature (known as homeotherms) from animals that do not (known as poikilotherms,  a personal favorite word of mine). The other axis separates endotherms, that is animals that use the heat generated by internal metabolic processes (such as muscle contraction) to warm their internal organs, versus ectotherms, that use environmental sources (most often the sun, but sometimes other sources such as hot springs) to heat themselves.
Now here's what's really fascinating. If you imagine a plot with these two axis, you will find organisms all over it. You will find ectotherms that are excellent homeotherms, and endotherms that are highly poikilothermic (many tropical marsupials fall in this category). What is more, most animals can occupy, depending on the environment they're in and the specifics of their physiology, multiple positions in this space.
Of particular interest to this debate are the many ocean going, highly active predatory fish that have evolved varying degrees of facultative endothermy. These are animals (such as tuna and sharks), that use a specific arrangement of blood vessels called a counter current exchanger to trap the heat generate by muscle activity in their swimming muscles, thus allowing them to keep those muscles at the best temperature for efficient function in cold water. The limitation of this strategy, however, is that eventually the heart cools down, slowing down its pumping rate and starving the muscles of oxygen.
Which is where the opah comes in. It flips the script on what other facultative endotherms do, and places the counter current exchanger in the gills (I urge to go and look at the paper now; the pictures of those gill counter current exchangers are breathtaking). As the gills are in direct contact with water, they are a major site of heat loss. Mammals and birds have similar problem in the respiratory system, and have independently evolved highly vascularised nasal turbinates which also use vascular counter current exchange to trap heat inside the body cavity during exhalation. By placing the counter current exchangers in its gills, the opah (if physicists will forgive me this inaccurate metaphor) traps the cold outside its body (thus brilliantly illustrating Claude Bernard's definition of homeostasis). Furthermore, evidence suggests that the opah may use its pectoral fin muscles purely to generate heat, rather than to aid in locomotion, thus fulfilling the strictest definition of endothermy (that is, the use of metabolic energy purely for the generation of heat). Finally, the opah has developed significant insulation the form of fat, so as to prevent heat loss through the skin. The upshot of all this is that the opah's internal organs, including its heart, remain considerably warmer than the surrounding water.
So it seems pretty clear the opah is probably a homeothermic endotherm, and probably a pretty good one. It is always exciting to see a completely unexpected organism have converged on an evolutionary solution that we thought only another organism had achieved. But what really got me excited was the discussion of why the opah might have evolved this form of life. Namely, facultative endotherms like tuna must eventually leave cold deep waters (which are rich in fish) for sun-warmed surface waters when their hearts cool down. The opah, through its metabolically expensive endothermy, can remain in those waters permanently. Why is this exciting? Because the exploitation of a cold environment is exactly the scenario that has been advanced for the evolution of endothermy in mammals. Namely, it has been suggested that mammalian endothermy allowed triassic mammals to hunt at night, when other, ectothermic amniotes would be sluggish. In the opah, we have validation of the hypothesis that endothermy can evolve so that a thermally constrained niche can be exploited.
Biology training is becoming increasingly narrow, yet also increasingly broad. We study systems in limited model organisms, and then expand the mechanisms across groups without consideration of the ecological, and evolutionary specificities that have made these organisms what they are. But if our evolutionary scenarios make sense, then we should expect them to be repeated: the biological equivalent of the old maxim that the same causes produce the same effects. In the opah, we find, unexpectedly, confirmation of our hypotheses on the ecological situations that underpin the evolution of endothermy. In the study of the opah's evolution, we may gain insight into the variety of thermoregulatory solutions that accompany such trends. Comparative physiology, broadly studied and understood, is full of unsuspected explanatory power.

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