Channichthyidae

Chionodraco hamatus

The crocodile icefish or white-blooded fish (Channichthyidae) comprise a family of notothenioid fish found in the Southern Ocean around Antarctica and southern South America, where water temperatures remain relatively stable (generally ranging from -1.8 to +2.0 °C).[2] Sixteen species of crocodile icefish are currently recognized.[3]

Diet and body size

All icefish are believed to be piscivorous but can also feed on krill.[4] Icefish are 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 have been recorded in these species.[5]

Respiratory and circulatory system

Hemoglobin

Icefish blood is colorless because it lacks hemoglobin, the oxygen-binding protein in blood.[3][6] 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.[7] In only one of the icefish species, Neopagetopsis ionah, there is a more complete, but still nonfunctional hemoglobin gene.[8]

Red blood cells (RBCs) are usually absent, and if present, are rare and defunct.[9] Oxygen is dissolved in the plasma and transported throughout the body without the hemoglobin protein. The fish can live without hemoglobin because of their 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).[3] However, the oxygen-carrying capacity of their blood is less than 10% that of their relatives with hemoglobin.[10]

Myoglobin

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.[11] Loss of myoglobin gene expression in icefish heart ventricles has occurred at least four separate times.[3][12]

Adaptations

To compensate for the loss of hemoglobin, they have larger blood vessels (including capillaries), greater blood volumes (four times that of other fish), bigger hearts, and greater cardiac outputs (fivefold greater) compared to other fish.[3] Their hearts lack coronary arteries, and the ventricle muscles are very spongy, enabling them to absorb oxygen directly from the blood they pump.[13] Their hearts, large blood vessels and low-viscosity (RBC free) blood are specialized to carry out very high flow rates at low pressures.[14] 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.[13] The little extra oxygen absorbed by the skin may play a part in supplementing the oxygen supply to the heart[13] which receives venous blood from the skin and body before pumping it to the gills.

Evolution

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.[3] Any adaptive advantages incurred by reduced blood viscosity are outweighed by the fact that icefishes must pump much more blood per unit of time so as to make up for the reduced oxygen-carrying capacity of their blood.[3] 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 damages to their impaired oxygen-binding and transport systems.

Loss of myoglobin

As discussed previously, phylogenetic relationships indicate that the expression of myoglobin in cardiac tissue has occurred at least four discrete times.[11] This repeated loss suggests that cardiac myoglobin might 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.[3] This means that it is unlikely that myoglobin would be selected against. These 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.[3] This finding suggests that fish without cardiac myoglobin have undergone compensatory adaptation.

Why did these traits fix if they are not adaptive?

Given that the loss of these oxygen-binding proteins was likely not adaptive, it is hard at first glance to fathom why the traits were not selected against. However, icefishes evolved under unusual circumstances, both environmentally and biologically.

Physical environment

The Antarctic 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.[15] 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.[6] The aforementioned 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 environment

Biological factors, in particular an unusually low level of interspecific competition, also contributed to the fixation of these unexpected traits. Part of this is because there was a severe crash in fish biodiversity sometime between the mid-Tertiary and the present.[16] Second, physical factors have contributed to the relative isolation of icefishes, including 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.

So, these traits managed to fix, not because they were adaptive but because conditions allowed for a maladaptive trait to not be selected against. Yet other compensatory mechanisms do appear to have fixed, suggesting the presence of some evolutionary pressure. This creates somewhat of a paradox.

How did icefishes' unique cardiovascular physiology evolve under conditions of reduced competition and evolutionary pressure?

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.[17] 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 went up in individuals.[3] 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.[18] The presence of nitric oxide also can increase angiogenesis, mitochondrial biogenesis, and cause muscle hypertrophy - all traits that 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.[3] 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, thereby providing a grace period of the fixation of these less than desirable traits.

Other evolutionary history

These fish have 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. 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 allowed for the loss of myoglobin.[3]

References

  1. ↑ Froese, Rainer, and Daniel Pauly, eds. (2013). "Channichthyidae" in FishBase. February 2013 version.
  2. ↑ Clarke, A (1990). "Temperature and evolution: Southern Ocean cooling and the Antarctic marine fauna". Antarctic Ecosystems: 9–22. doi:10.1007/978-3-642-84074-6.
  3. 1 2 3 4 5 6 7 8 9 10 11 12 Sidell, Bruce D; Kristin M O'Brien (2006-05-15). "When Bad Things Happen to Good Fish: The Loss of Hemoglobin and Myoglobin Expression in Antarctic Icefishes". Journal of Experimental Biology. 209 (10): 1791–1802. doi:10.1242/jeb.02091. ISSN 0022-0949. PMID 16651546. Retrieved 2012-04-07.
  4. ↑ LaMesa, Mario (2004). "The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review". Polar Biology. 27: 321–338. doi:10.1007/s00300-004-0599-z.
  5. ↑ Artigues, Bernat (2003). "Fish length-weight relationships in the Weddell Sea and Bransfield Strait". Polar Biology. 26: 463–467. doi:10.1007/s00300-003-0505-0.
  6. 1 2 Ruud, Johan T. (1954-05-08). "Vertebrates without Erythrocytes and Blood Pigment". Nature. 173 (4410): 848–850. doi:10.1038/173848a0. PMID 13165664. Retrieved 2012-04-07.
  7. ↑ Cocca, E (1997). "Do the hemoglobinless icefishes have globin genes?". Comp. Biochem. Physiol. A. 118: 1027–1030. doi:10.1016/s0300-9629(97)00010-8.
  8. ↑ Near, T. J.; Parker, S. K.; Detrich, H. W. (2006). "A genomic fossil reveals key steps in hemoglobin loss by the antarctic icefishes". Molecular Biology and Evolution. 23 (11): 2008–2016. doi:10.1093/molbev/msl071. PMID 16870682.
  9. ↑ Barber, D. L; J. E Mills Westermann; M. G White (1981-07-01). "The blood cells of the Antarctic icefish Chaenocephalus aceratus Lönnberg: light and electron microscopic observations". Journal of Fish Biology. 19 (1): 11–28. doi:10.1111/j.1095-8649.1981.tb05807.x. ISSN 1095-8649.
  10. ↑ Holeton, George (2015-10-15). "Oxygen uptake and circulation by a hemoglobinless Antarctic fish (Chaenocephalus aceratus Lonnberg compared with three red-blooded Antarctic fish". Comparative Biochemistry and Physiology. 34: 457–471.
  11. 1 2 Sidell, B. D.; Vayda, M. E.; Small, D. J.; Moylan, T. J.; Londraville, R. L.; Yuan, M. L.; Rodnick, K. J.; Eppley, Z. A.; Costello, L.; et al. (1997). "Variable expression of myoglobin among the hemoglobinless antarctic icefishes". Proceedings of the National Academy of Sciences of the United States of America. 94 (7): 3420–3424. doi:10.1073/pnas.94.7.3420. PMC 20385Freely accessible. PMID 9096409.
  12. ↑ Grove, Theresa (2004). "Two species of Antarctic icefishes (Genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression". Polar Biology. 27: 579–585. doi:10.1007/s00300-004-0634-0.
  13. 1 2 3 Rankin, J.C; H Tuurala (January 1998). "Gills of Antarctic Fish". Comparative Biochemistry and Physiology A. 119 (1): 149–163. doi:10.1016/S1095-6433(97)00396-6. ISSN 1095-6433. Retrieved 2012-04-09.
  14. ↑ Tota, Bruno; Raffaele Acierno; Claudio Agnisola; Bruno Tota; Raffaele Acierno; Claudio Agnisola (1991-06-29). "Mechanical Performance of the Isolated and Perfused Heart of the Haemoglobinless Antarctic Icefish Chionodraco Hamatus (Lonnberg): Effects of Loading Conditions and Temperature". Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 332 (1264): 191–198. doi:10.1098/rstb.1991.0049. ISSN 0962-8436. Retrieved 2012-05-18.
  15. ↑ Kennett, J. P. (1977). "Cenozoic evolution of Antarctic glaciation, the circus-Antarctic Ocean and their impact on global paleooceanography.". Journal of Geophysical Resources. 82.
  16. ↑ Eastman, J. T. (2005). "The nature of the diversity of Antarctic fishes.". Polar Biology. 28.
  17. ↑ Gardner, P. R. (2004). "Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin, and their associated reductases.". Journal of Inorganic Biochemistry. 99.
  18. ↑ Pellegrino, D., R. Acierno, and B. Tota (2003). "Control of cardiovascular function in the icefish Chionodraco hamatus: involvement of serotonin and nitric oxide.". Computational Biochemical Physiology. 134A.
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