T. N. Gill, 1861
The crocodile icefish or white-blooded fish (Channichthyidae) comprise a family of notothenioid fishes found in the Southern Ocean around Antarctica. They are the only known vertebrates to lack hemoglobin in their blood as adults. Icefish populations are known to reside in the Atlantic and Indian sectors of the Southern Ocean as well as the continental shelf waters surrounding Antarctica. Water temperatures in these regions remain relatively stable, generally ranging from −1.8 to 2 °C (28.8 to 35.6 °F). One icefish, Champsocephalus esox, is distributed north of the Antarctic Polar Frontal Zone. At least sixteen species of crocodile icefish are currently recognized, although eight additional species have been proposed for the icefish genus Channichthys.
- 1 Diet and body size
- 2 Respiratory and circulatory system
- 3 Evolution
- 4 References
- 5 External links
Diet and body size
All icefish are believed to be piscivorous but can also feed on krill. Icefish are typically ambush predators; thus, they can survive long periods between feeding and often consume fish up to 50% of their own body length. Maximum body lengths of 25–50 cm (9.8–19.7 in) have been recorded in these species.
Respiratory and circulatory system
Icefish blood is colorless because it lacks hemoglobin, the oxygen-binding protein in blood. Channichthyidae are the only known vertebrates to lack hemoglobin as adults. Although they do not manufacture hemoglobin, remnants of hemoglobin genes can be found in their genome. The hemoglobin protein is made of two subunits (alpha and beta). In 15 of the 16 icefish species, the beta subunit gene has been completely deleted and the alpha subunit gene has been partially deleted. One icefish species, Neopagetopsis ionah, has a more complete, but still nonfunctional hemoglobin gene.
Red blood cells (RBCs) are usually absent, and if present, are rare and defunct. Oxygen is dissolved in the plasma and transported throughout the body without the hemoglobin protein. The fish can live without hemoglobin via low metabolic rates and the high solubility of oxygen in water at the low temperatures of their environment (the solubility of a gas tends to increase as temperature decreases). However, the oxygen-carrying capacity of icefish blood is less than 10% that of their relatives with hemoglobin.
Myoglobin, the oxygen-binding protein used in muscles, is absent from all icefish skeletal muscles. In 10 species, myoglobin is found in the heart muscle, specifically ventricles. Loss of myoglobin gene expression in icefish heart ventricles has occurred at least four separate times.
To compensate for the loss of hemoglobin, icefish have larger blood vessels (including capillaries), greater blood volumes (four-fold those of other fish), larger hearts, and greater cardiac outputs (five-fold greater) compared to other fish. Their hearts lack coronary arteries, and the ventricle muscles are very spongy, enabling them to absorb oxygen directly from the blood they pump. Their hearts, large blood vessels and low-viscosity (RBC-free) blood are specialized to carry out very high flow rates at low pressures. This helps to reduce the problems caused by the lack of hemoglobin. In the past, their scaleless skin had been widely thought to help absorb oxygen. However, current analysis has shown that the amount of oxygen absorbed by the skin is much less than that absorbed through the gills. The little extra oxygen absorbed by the skin may play a part in supplementing the oxygen supply to the heart which receives venous blood from the skin and body before pumping it to the gills.
The icefishes are considered a monophyletic group and likely descended from a sluggish demersal ancestor. The cold, well-mixed, oxygen-rich waters of the Southern Ocean provided an environment where a fish with a low metabolic rate could survive even without hemoglobin, albeit less efficiently.
It is still unknown when the icefish evolved, but there are two main competing hypotheses. The first is that they are only about 6 million years old, appearing after the Southern Ocean cooled significantly. The second predicts that they are much older, evolving 15-20 million years ago.
Although the evolution of icefish is still disputed, it is widely accepted that the formation of the Antarctic Polar Frontal Zone (APFZ) and the Antarctic Circumpolar Current (ACC) marks the beginning of the evolution of Antarctic fishes. The ACC is an oceanic current that moves in a clockwise northeast direction, and can be up to 10,000 km (6,200 mi) wide. This current formed 25-22 million years ago, and thermally isolated the Southern Ocean by separating it from the warm subtropical gyres to the north.
During the mid-Tertiary period, a species crash in the Southern Ocean opened up wide range of empty niches to colonize. Despite the hemoglobin-less mutants being less fit, the lack of competition allowed even the mutants to leave descendants that colonized empty habitats and evolved compensations for their mutations. Later, the periodic openings of fjords created habitats that were colonized by a few individuals. These conditions may have also allowed for the loss of myoglobin.
Loss of hemoglobin
The loss of hemoglobin was initially believed to be an adaptation to the extreme cold as the lack of hemoglobin and red blood cells decreases blood viscosity, which is an adaptation that has been seen in species adapted to cold climates. However, current analysis has shown that the lack of hemoglobin, while not lethal, is not adaptive. Any adaptive advantages incurred by reduced blood viscosity are outweighed by the fact that icefishes must pump much more blood per unit of time in order to make up for the reduced oxygen-carrying capacity of their blood. The high blood volume of icefishes is itself evidence that the loss of hemoglobin and myoglobin was not advantageous for the ancestor of the icefishes. Their unusual cardiovascular physiology, including large heart, high blood volume, increased mitochondrial density, and extensive microvasculature, suggests that icefishes have had to evolve ways of coping with the impairment of their oxygen binding and transport systems.
Loss of myoglobin
Phylogenetic relationships indicate that the non-expression of myoglobin in cardiac tissue has evolved at least four discrete times. This repeated loss suggests that cardiac myoglobin may be vestigial or even detrimental to icefishes. Sidell and O'Brien (2006) investigated this possibility. First, they performed a test using stopped-flow spectrometry. They found that across all temperatures, oxygen binds and dissociates faster from icefish than it does from mammalian myoglobin. However, when they repeated the test with each organism at a temperature that accurately reflected its native environment, the myoglobin performance was roughly equivalent between icefishes and mammals. So, they concluded that icefish myoglobin is neither more nor less functional than the myoglobin in other clades. This means that it is unlikely that myoglobin would be selected against. The same researchers then performed a test in which they selectively inhibited cardiac myoglobin in icefishes with natural myoglobin expression. They found that icefish species that naturally lack cardiac myoglobin performed better without myoglobin than did fish that naturally express cardiac myoglobin. This finding suggests that fish without cardiac myoglobin have undergone compensatory adaptation.
Reason for trait fix
Given that the loss of these oxygen-binding proteins was likely not adaptive, it is difficult at first glance to fathom why the traits were not selected against. However, icefishes evolved under unusual circumstances, both environmentally and biologically.
The Southern Ocean is an atypical environment. To begin with, the Southern Ocean has been characterized by extremely cold but stable temperatures for the past 10-14 million years. These cold temperatures, which allow for higher water oxygen content, combined with a high degree of vertical mixing in these waters, means that there is unusually high oxygen availability in Antarctic waters. For a fish that has lost its oxygen-binding proteins, this is a most fortuitous property. The loss of hemoglobin and myoglobin would have negative consequences in warmer environments. The stability in temperature is also "lucky," as strong fluctuations in temperature would create a more stressful environment that would likely weed out individuals with deleterious mutations.
Biological factors, in particular an unusually low levels of interspecific competition, also contributed to the fixation of these unexpected traits. This lack of competition resulted in part from a severe crash in fish biodiversity sometime between the mid-Tertiary and the present. Additionally, several physical factors have contributed to the relative isolation of icefishes; these include circumpolar currents, trenches that surround the Antarctic continent, and, throughout the past 5 million years, the sporadic presence of refugia in the form of ice-free marine embayments.
Consequently, these traits became fixed, not because they were adaptive but because conditions allowed for a maladaptive trait to not be selected against. In contrast, other compensatory mechanisms do appear to have been fixed, suggesting the presence of some evolutionary pressure. This creates somewhat of a paradox.
The key to solving this conundrum is to consider the other function that both hemoglobin and myoglobin perform. While emphasis is often placed and understandably so on the importance of hemoglobin and myoglobin in oxygen delivery and use, recent studies have found that both proteins are actually also involved in the process of breaking down nitric oxide. This means that when icefishes lost hemoglobin and myoglobin, it did not just mean a decreased ability to transport oxygen, but it also meant that total nitric oxide levels were elevated. Nitric oxide plays a role in regulating various cardiovascular processes in icefishes, such as the dilation of branchial vasculature, cardiac stroke volume, and power output. The presence of nitric oxide also can increase angiogenesis, mitochondrial biogenesis, and cause muscle hypertrophy; all of these traits are characteristic of icefishes. The similarity between nitric oxide-mediated trait expression and the unusual cardiovascular traits of icefishes suggests that while these abnormal traits have evolved over time, much of these traits were simply an immediate physiological response to heightened levels of nitric oxide, which may in turn have led to a process of homeostatic evolution. In addition, the heightened levels of nitric oxide that followed as an inevitable consequence of the loss of hemoglobin and myoglobin may have actually provided an automatic compensation, allowing for the fish to make up for the hit to their oxygen transport system and thereby providing a grace period of the fixation of these less than desirable traits.
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