Thunniform swimming depends on a large, lunate tail that is joined to the rest of the body via a narrow peduncle. Whilst the tail flicks backwards and forwards, so propelling the animal, the rest of the body hardly moves sideways.

It comes as no surprise to see that large marine animals that swim fast, typically range very widely (sometimes for thousands of kilometres) and can often dive to considerable depths, typically have a fusiform body, a prominent tail and stabilizing fins. Familiar examples include many marine mammals including dolphins, the extinct ichthyosaurs, the sharks and tuna. In the last two cases, however, there is a very striking convergence that, as Jeanine Donley and colleagues rightly emphasize, is much more than skin deep. In the case of the sharks the particular comparison rests on the lamnids, although a similar case applies also to the somewhat less well-known alopiid sharks.

Thunniform swimming in lamnid sharks and tuna

Both tuna and shark progress by what is known as thunniform swimming. In essence this depends on a large, lunate tail that is joined to the rest of the body via a narrow peduncle. Whilst the tail flicks backwards and forwards, so propelling the animal, the rest of the body hardly moves sideways. This is in marked contrast to most fish which locomote by throwing the body into a series of sinous waves, generally referred to as carangiform and is at its most pronounced in the angulliform locomotion of the eels. In all cases, of course, the locomotory power is provided by the muscular contractions, but in thunniforms the power is transmitted to the tail in a very specific fashion.

It is necessary to know that in fish there are typically two types of muscle. Usual locomotion is achieved by contraction of aerobic red muscle that is usually located on the body margins, and whose contractions can throw the body into sinous waves. The white muscle is only used for power bursts, and because it can function without oxygen it is referred to as anaerobic. Understandably power bursts can only be of short duration because the oxygen debt has to be paid off (a direct analogy is the build-up of lactic acid in our calf muscles when we run too fast for the legs to be supplied with enough oxygen). In lamnid sharks and tuna, the fish have independently arrived at an almost identical solution to achieve thunniform locomotion. The main mass of red muscle is moved more centrally, and becomes largely independent of the rest of the muscle blocks so when it contracts it slides semi-independently. Second, and critically, the power of the muscular contractions is transmitted to the tail via a system of tendons. Crucially, although the function of the tendons is effectively identical, their origin in lamnid sharks is different from that of tuna. Thus, as ever, there is an evolutionary footprint.

Thermoregulation in sharks and tuna

Another key innovation of this system is the independent evolution of thermoregulation and endothermy (“warm-bloodedness”). Endothermy has evolved independently many times e.g. in other vertebrates such as birds and mammals, and also many groups of insects, such as the sphingid moths. The principle area of heat generation in endothermic fish is in the alimentary canal, but heat is generated in different regions in the shark and tuna. Secondary areas of heat generation are also found in the brain and eye regions of sharks and tuna, and it is possible that this assists visual acuity and cognition, at least in the shark.

One critical anatomical feature in the endothermy of shark and tuna is the evolution of a counter-current blood system. Typically, this consists of a network of blood vessels (rete mirabile, or “wonderful network”) whereby blood flowing in either direction can exchange heat (or in cases such as the fish swim bladder, respiratory gases). In effect, heat that is being transported out of the zone of thermal generation is constantly transported back so as to maintain a core temperature higher than other areas of the body. This has a potentially disastrous consequence because the solubility of oxygen decreases with increasing temperature, so the warmth that is being returned to the core region by the blood flow ought to contain less oxygen, a hardly helpful development given that this is a region of high metabolic activity. The trick to solve this physiological problem has been to induce a so-called reverse temperature effect in the haemoglobin (the protein that carries the oxygen), and unsurprisingly this has evolved independently in shark and tuna.