Biochemical Soul Musings on Nature, Science, Evolution, Biology, and Education

25Mar/09Off

Adaptation of the Week – Channichthyidae Icefish Blood and Antifreeze

I owe the following example of evolutionary adaptation to the always amazing evolutionary and developmental biologist Dr. Sean B. Carroll, from his lecture "Making of the Fittest" for the Darwin College - Darwin Lecture Series, available at iTunes U (I highly recommend everyone give it a listen).

The Red Blood Cell-less Icefish © Dr Julian Gutt and Alfred Wegener Institute

The Red Blood Cell-less Icefish © Dr Julian Gutt and Alfred Wegener Institute

Imagine that you are a fish - exothermic and thus unable to regulate your own body temperature - and the contingent foibles of natural history have all conspired to leave you and your kind in the frigid oceans of the Antarctic just as they are beginning to reach the freezing point (10-14 million years ago).

You like the cold and are well adapted for it, but these temperatures are beginning to give even you - a master of the cold - the icthy chills.

Now imagine that the hands of mother nature have given you the tools to change your own genetic code, and thus your nature, allowing you to make yourself even more suited for waters that are 2 degrees celsius below the freezing point of pure water.

What would you do? Would you inject your DNA with a molecular antifreeze? That seems like a reasonable addition - one we will get to momentarily.

But if you were a genius of bioengineering would you reach out a molecular scalpel and hack away the genes that allow the production of red blood cells, hemoglobin, and myoglobin, leaving only molecular fossils behind?

Icefish Larva

Icefish Larva © Uwe Kils

It doesn't seem like a particularly well thought out plan. But then again, neither you, the fish, nor mother nature are genius bioengineers. Fortunately for life, the forces of evolution still manage to get the job done, however sloppy the end results (yes, technically the job is never done - forgive my metaphor wearing thin).

In fact, natural selection performed just such a feat somewhere around 8.5 million years ago in the ancestors of a flock of related species in the Antarctic: the Channichthyidae icefishes (also known as crocodile icefishes or white-blooded fishes).

As we all know, liquids tend to become more viscous in the cold. Just compare maple syrup before and after refrigeration. Blood viscosity would have no doubt been an issue in the ancient ice fish ancestors, or at least one that could be improved upon. Normal vertebrate blood is filled with big, round, and red blood cells coursing through the blood vessels. Now imagine lowering the temperature of the blood below the normal freezing point of water - that's bound to create some significant resistance.

But aren't erythrocytes critical for carrying oxygen? How could an organism just dispense with them completely? As many scientists know, one of the great things about really cold water is that it can be packed with oxygen. Such is the case with the waters of the Southern Ocean, which are saturated with oxygen.

Thus, it seems that at some point, the icefish ancestors developed mutations in the pathways that result in red blood cell production. Furthermore, the species eventually acquired a deletion in the key genes of red blood cells: the alpha and beta hemoglobin genes. No longer could this fish produce hemoglobin.

As is often the case with evolution through loss of gene function, the deletion wasn't perfect. Almost all vertebrates have both hemoglobin genes lying next to each other within the genome. In most Channichthyidae icefishes, the beta hemoglobin gene has been completely deleted, along with all but the truncated end of the alpha hemoglobin gene (interestingly, these fish have lost their myoglobin gene as well)1. To quote the original paper by Near et al.:

"Despite the costs associated with loss of hemoglobin and myoglobin in icefishes, the chronically cold and oxygen-saturated waters of the Southern Ocean provided an environment in which vertebrate species could flourish without oxygen-binding proteins."

The upshot of all this is that the icefish has completely clear blood lacking in any erythrocytes - and they are the only species of vertebrates to have such a trait.

Normal 2 globin genes vs. lost icefish globins - modified from Near et al 2006

Normal two hemoglobin genes vs. lost icefish hemoglobins - cropped figure from Near et al 2006

Of course, a few other supporting traits evolved as well. Their hearts are significantly larger than other fish hearts, and they pump 4 to 5 times larger volume of blood per stroke2. Their capillary beds have become much more dense as well to make sure all their tissues get adequate oxygenation. Of course, like amphibians that breathe through their skin, with the loss of red blood cells, those that were better able to absorb oxygen tended to outperform their cohorts. Thus they became scaleless as well.

As if these adaptive feats weren't cool enough (pun intended), the antarctic icefishes have evolved their own antifreeze as well3,4. What's amazing about this antifreeze (an Antifreeze Glycoprotein - or "AFGP") is that it represents one clear cut case in which a gene with a specific function has evolved into a separate gene used for a completely different function in a novel way. In the case of the icefish, the ancestral gene was a trypsinogen (a pancreatic digestive enzyme), which has been mutated and co-opted to be secreted and distributed throughout the body to act as an antifreeze. Specifically (for you biologists out there), the 5' secretory signal and 3' UTR sequences of trypsinogen were tacked onto an amplified nine nucleotide sequence from within the trypsinogen precursor to create the novel antifreeze peptide.

So here we have in the icefish's adaptation to the cold, at least one case of de novo creation of a novel gene with a new function from an old gene, as well as the loss of two other genes that have left genomic fossils behind to whither in the weathers of time.

It may not be the cleanest or best engineered solution to the problem of living in an Antarctic Hell (or perhaps Heaven from the perspective of the fish), but this messiness of evolution is precisely what makes it so incredibly beautiful.

References

  1. Near T.J., Parker S.K.,  Detrich H.W. A genomic fossil reveals key steps in hemoglobin loss by the Antarctic icefishes. Molecular Biology and Evolution, v.23, 2006, p. 2008 - 2016.
  2. William C. Aird. Endothelial biomedicine. Edition: illustrated. Published by Cambridge University Press, 2007
  3. Chen L., DeVries A.L., Cheng C-H. C. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid?fish. PNAS, April 15, 1997 vol. 94 no. 8 3811-3816
  4. Chen L., DeVries A.L., Cheng C-H. C. Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic?cod. PNAS, April 15, 1997 vol. 94 no. 8 3817-3822
  5. Top image © Dr Julian Gutt and Alfred Wegener Institute
  6. Icefish larval image by Uwe Kils

Previous Adaptations of the Week:

  1. Timber Rattlesnake Camoflage
  2. The Aye-Aye’s Freaky Finger (I’ve Been Cursed by an Aye-Aye!)
  3. Flatfish Eyes & Recapitulation Theory
  4. Bird/Crocodile Symbiosis?
  5. Insect Dorsal Ocelli
Comments (12) Trackbacks (2)
  1. It’s not at all clear that the loss of red blood cells in icefish is an adaptation. Here is a quick summary of why (Sidell & O’Brien 2006):

    On average, icefishes expend approximately twice the cardiac energy per unit time than do red-blooded notothenioids of equivalent body mass. Although each ml of blood can be moved by icefish at lower energetic cost, they pump a far greater volume per unit time to support an equivalent body mass. …

    In light of these energetic considerations and the rather draconian compensatory alterations in cardiovascular anatomy and physiology seen in icefishes, it seems reasonable to conclude… that loss of Hb and red cells did not confer an adaptive advantage to the channichthyids.

    In fact, the loss of these cells may be one of the best cases of a disaptation, which is a feature in a species that is notably worse than its ancestor had (Montgomery & Clements 2000).

    Disaptations are expected to be rare, but rare does not mean unimportant.

    Shameless self-promotion: I recently published an article discussing how disaptations could actually drive diversification (Faulkes 2008).

    References

    Faulkes Z. 2008. Turning loss into opportunity: The key deletion of an escape circuit in decapod crustaceans. Brain, Behavior and Evolution 72(4): 251-261.
    doi: 10.1159/000171488

    Montgomery J, Clements K. 2000. Disaptation and recovery in the evolution of Antarctic fishes. Trends in Ecology and Evolution 15: 267 -271. doi: 10.1016/S0169-5347(00)01896-6

    Sidell BD, O’Brien KM. 2006. When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes. The Journal of Experimental Biology 209: 1791-1802. doi: 10.1242/jeb.02091

    • I really appreciate your comments – as I am far from an expert on these fish.

      I guess one of the main questions I have (I haven’t read your references yet but I definitely will) is whether it could be considered adaptive by definition because the alleles that resulted in loss of hematopoiesis spread through the entire population (and almost all daughter species over time).

      If it were not adaptive, would not it have been outcompeted by the rest of the population?

      Well, obviously if some singular event (Gould’s “decimation”) caused a bottleneck such that only the white-blooded individuals survived, I could see how a maladaptive trait would succeed. Is this the mechanism through which you think this maladaptation evolved?

      Thoughts?

      (I realize your citations probably answer this – but can you give a quick synopsis anyway?)

      • I’m not an expert on fish, either. Unless crayfish count. 😉

        Could it be adaptive by definition because the alleles spread through the entire population?

        My quick response is that under a definition like that, absolutely everything becomes adaptive, and the word loses any useful meaning.

        To me, adaptation is concerned with demonstrated survival value or reproductive benefit than population genetics.

        Adaptation is, quite reasonably, the default explanation for organismal features. It’s what theory predicts. But as Gould and Lewontin (1979) argued, adaptation isn’t the only game in town.

        Reference

        Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London. Series B 205: 581-598.

    • P.S. I haven’t read them yet because I don’t have journal access at home.

    • Alright – finally got my computer fixed so I can answer.

      I read both of the two articles today concerning the putative “disaptive” nature of Hemoglobin (Hb) and Myoglobin (Mb) loss.

      First I should state that I have no problem whatsoever with the concept of specific molecular events resulting in disaptations. I would be more surprised if such events were never found considering the somewhat chaotic nature of…nature. Again, this fits in with my point above that evolution is usually messy.

      Now, I have to say that I have some real problems with the logic in the primary article that postulates that Hb loss was a detrimental change. Let me make it clear that these are only my opinions from a couple of readthroughs of the literature concerned – and I have no problem conceding that I might be totally wrong – so feel free to argue.

      1) The first problem is what I see as a general mistake the authors make throughout the paper. They continuously use comparisons between modern white-blooded icefishes and modern red-blooded icefishes to try to make conclusions about the relationship between the fish that originally lost Hb and its relatives that did not.

      For example, they show that icefish of today expend more energy in distributing oxygen than modern red-blooded relatives.

      But I think it is a leap to take this finding and extrapolate that it must have been bad for those first fish to lose Hb, under what may have been significantly different conditions.

      This may have been the case, but their evidence is far from proving it.

      2) The authors use only the energy consumption of the cardiovascular system and metabolism as the defining metric for adaptation. No doubt this is a major factor in an individuals success, but it is not hard to imagine that the energy demands might have been outweighed by other effects of Hb loss. I don’t think our understanding of all the physiological effects of such a gene loss (including secondary effects and how they might have affected reproductive success) is anywhere near complete enough to conclude that Hb loss was necessarily detrimental.

      3) They make a big deal of arguing that nitric oxide (NO) effects, cardiac enlargement, capillary dilation and density increase are all due to the fish making up for the loss of Mb (and Hb), which they also claim was deleterious. Yet they also show that Mb should work fine at cold temperatures (i.e. Mb didn’t just erode due to uselessness) AND that Mb loss occurred independently multiple times in various icefish lineages.

      Sure, you could argue that what little we understand of Mb and it’s connection to NO production and cardiovascular physiology argues that Mb loss was a disadvantage.

      However, Occam’s razor (combined with what we already understand about natural selection) leads me to lean toward an explanation that Mb loss gave these fish some adaptive advantage in the frigid Southern Ocean to leave behind more pffspring. Why else would multiple lineages just happen to lose Mb (each via different mutations), AND result in each of those mutations spreading through that particular species population?

      Basically, I think their ideas and data are intriguing – but it’s a far cry from what it would take to prove that the original mutational events were disadvantageous in those ancient species living under different physiological, ecological, and environmental conditions.

  2. To respond to Daniel’s question, not necessarily – it’s possible that any mutation/deletion/etc, even a disadaptive one, spreads if…

    The organism has other traits which it ‘bests’ its companions in (ie deletion occurred in the guy with the biggest testes or something, completely unrelated to each other). Anything that out-performs the “bad” caused by the deletion.

    Or, technically, there could have been a random genetic shift like you said. Not entirely likely, but possible.

    Or, it’s possible that something about the deleted gene isolated that population from the rest – maybe it prompted a change in behavior or something, so that the deleted gene guys usually could only get with deleted gene girls. Soon enough you have an ancestral deleted-gene species, even though there’s nothing “positive” about the deletion. The other species moved more equatorially to avoid the cold and either developed into something totally different or died off for other reasons.

  3. [rubbing hands together with look of evil satisfaction that daniel continues to feature oceanic exemplars]

    if i might toss a comment into this thread that follows-up on zen’s comments, i’d have to agree that in my mind adaptation is concerned with demonstrated survival value or reproductive benefit… given that, it becomes a tougher sell for me to see loss of red blood cells in icefish as a spandrel (merely an architectural byproduct of fish evolution in deep, cold habitats)… that being said, i’ve also not read the citations zen provided so can’t comment further…

    i would like to point out, however, that i think steve gould would have gotten a kick out of the use of “disaptation”… as zen points out from the citation of the seminal gould/lewontin paper, steve was always cautious and critical of hyper-adaptationist thinking…

    i consider myself fortunate enough to have been a grad student in several of his macroevolution seminars, and i can speak from experience that whenever anyone would utter “pre-adaptation” or even “exaptation” steve would perform his characteristic heavy squinting accompanied by vigorous shaking of his head in disgust… this from the man who coined “exaptation” with elizabeth vrba…

    i think “disaptation” would have given him conniptions too…

  4. Interesting write up Daniel and really nice to see some active discussion on adaption…….. But as i am not an expert on this ………;so better i read the references provided and then say something…….anyways many thanks for the comment on unrulednotebook.wordpress.com/2009/03/26/indian-scientists-and-science-blogging/ ……..and i am an Indian only….infact u made a correct guess ……sean carroll’s talk was really nice …thanks for the info ………..

  5. I don’t know enough to jump in to the discussion above, but I definitely enjoyed the article and the discussion and will be back for more. I enjoyed meeting you last night at dinner – would like to meet up again whenever we’re both in Pittsburgh

  6. I liked the article too, because I just revisited Sean B. Carroll’s The Making of the Fittest.