Coelacanth genome sequenced

by Greg Mayer

Coelacanths are one of the three surviving groups of sarcopterygian (lobe-finned) fishes, and along with lungfish, one of the two groups that have remained fish in the vernacular sense (we tetrapods, the third surviving group, have of course become legged). The coelacanths also have a tremendous back story: known in the fossil record from the Devonian (over 350 mya) till the end of the Mesozoic Era (about 65 mya) but not afterward, it came as a great shock when one popped up in South Africa in 1938.

Latimeria chalumnae, the coelacanth (model)

Latimeria chalumnae, the coelacanth (model). Notice lobed fins.

Marjorie Courtenay-Latimer, curator of the local museum, got it at the fishing wharf in East London, Cape Province, where a fishing captain had put it aside for her as an unusual specimen. The discovery of a living specimen of a fish long thought extinct, and one related to tetrapods to boot, was a worldwide sensation. Others eventually turned up at various points in the western Indian Ocean, and in 1998 a population was discovered in Indonesia at the opposite end of the Indian Ocean.

Yesterday, a group led by Chris Amemiya (and including friend-of-this-site Neil Shubin) published the genome sequence of the coelacanth in the journal Nature. It is open access, and remarkably long and detailed given Nature‘s cramped editorial style. To me, two things stand out after a quick look. First, the coelacanth is the next closest relative to the tetrapods, after the lungfish. This is what was expected, but the paper provides much stronger support for this, using a  large data set (251 judiciously chosen genes). Note that, in an especially nice touch, Homo sapiens is represented in the figure by Miss Courtenay-Latimer herself.

Phylogenetic tree using coelacanth genomic data (Fig. 1 from Amemiya etal. 2013).

Phylogenetic tree using coelacanth genomic data (Fig. 1 from Amemiya etal. 2013).

Second, although, slightly more distantly related genealogically to tetrapods than lungfish, the slowly evolving coelacanths provide better comparisons for inferring events in early tetrapod genomic evolution than do the highly genomically derived lungfish. As Ammemiya et al. put it,

The vertebrate land transition is one of the most important steps in our evolutionary history. We conclude that the closest living fish to the tetrapod ancestor is the lungfish, not the coelacanth. However, the coelacanth is critical to our understanding of this transition, as the lungfish have intractable genome sizes (estimated at 50–100Gb)47. Here we have examined vertebrate adaptation to land through coelacanth whole-genome analysis, and have shown the potential of focused analysis of specific gene families involved in this process. Further study of these changes between tetrapods and the coelacanth may provide important insights into how a complex organism like a vertebrate can markedly change its way of life.

This is a bit reminiscent to the situation in studies of vertebrate origins: it now seems clear that sea squirts (urochordates) are closer genealogically to vertebrates than lancelets (cephalochordates), yet lancelets provide better comparative material for investigating early vertebrate evolution than do the highly derived sea squirts.

______________________________________________________________

Amemiya, C., et al. 2013. The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311-316. (pdf)

Holland, P. 2006 My sister is a sea squirt? Heredity 96:424–425. (pdf)

42 Comments

  1. Posted April 19, 2013 at 4:23 pm | Permalink

    I have that model!

    Fascinating stuff.

    /@

  2. Posted April 19, 2013 at 4:32 pm | Permalink

    i love stories like that, they make me feel truly ancient, especially so since i used to have a vestigal gill, one line of the family does, which however becomes infected in childhood or adolescence and then needs to be removed as a kind of cyst.

    • Posted April 19, 2013 at 4:41 pm | Permalink

      But the real question is: does it taste good?

      • Mark Joseph
        Posted April 20, 2013 at 12:02 pm | Permalink

        See the post below on the book “A Fish Caught in Time.” Both this book and every other source I’ve ever seen about the Coelacanth indicates that it does not taste good, which is probably why it is not extinct.

    • Torbjörn Larsson, OM
      Posted April 20, 2013 at 4:33 am | Permalink

      I don’t know how to put this without implying personal criticism, but I find this troubling. I’ve heard of vestigial gill slits (pharyngeal grooves), but gills?

      “Approximately one month after conception, the human embryo has a series of 4 bumps that appear about where you`d think the front of the neck should be. At this time of development the facial structures aren`t very well formed. These bumps are called “pharyngeal arches.” They go on to develop into the muscles of the face and neck, the salivary glands, nerves of the face and neck, and the bones of the middle ear and throat. Fish embryos have these same bumps but, in fish, they develop into the gills.

      As you look at the human embryo, there are slits between these bumps (“pharyngeal grooves”). The remains of the first groove can be found after we`re born as the opening into the ear canal. The other grooves usually disappear as the neck develops.

      If a pharyngeal groove does not completely disappear, it may be seen in a person as a small tunnel or pit in the skin of the side of the neck — usually near the edge of the long strap muscles that go from the corner of the jaw to the collarbone. The tunnel may end blindly or it may connect to the back of the throat near the tonsils. This is called a “branchial sinus”.

      A branchial sinus may have mucous come out of it. If the sinus becomes blocked, the mucous may become infected which will cause swelling and pain. This is probably what your staff member is referring to as “dirt in her gill”.”

      [ http://www.netwellness.org/question.cfm/15360.htm ]

      So do some individuals also develop the actual gills? (Anything can happen.)

      Or are we still talking gill slits and their existence as a frequent locus for infections? (The most likeliest events happens most, well, duh.)

      • Torbjörn Larsson, OM
        Posted April 20, 2013 at 4:35 am | Permalink

        I guess I should have worded that as “I don’t _mean_ to imply personal criticism…”. Alas, I’m still on the day’s first coffee here.

        Apologies.

      • Torbjörn Larsson, OM
        Posted April 20, 2013 at 4:47 am | Permalink

        And when I look at this again (okay, I’ve already started on the 2nd cup of coffee, maybe some more neurons are behaving as they should):

        I don’t see how a development program that according to the brief description in the medical text takes the arches and do other, derived, stuff with them (muscles, gland, nerves and bones) also manages to keep an ancestral structure. While the grooves, which are on the developmental path to disappear, are under less constraint.

        So arches (vs grooves) would be odd, but I guess still possible. (Armchair “biologist” here.)

        • Marcoli
          Posted April 20, 2013 at 6:14 am | Permalink

          There are many other features of air breathing tetrapod embryos that are similar to the branchial arches and grooves. For convenience, we can refer to these embryonic features as ‘primitive’, which are later remolded or replaced by other structures that are ‘derived’. We form the primitive notochord, a series of primitive kidneys, and unused extra-embryonic membranes like the allantois sac and yolk sac.
          None of these structures are used entirely as our ancestors did. So why have them? The likely answer seems to be that they provide an interactive environment that other structures need for their development– and we need those other structures. For example the notochord provides inductive signals that are needed by the adjacent somites and neural tube for their normal development. We still need our somites and neural tube, so we still need the interactive induction signals provided by the embryonic notochord.

        • Posted April 20, 2013 at 7:17 am | Permalink

          What can I say? I am mereley reporting my physician’s statement, provided many years after the opeation, at age 6,in Vienna – for half a year I had a brick red tube stuck in the left side of my neck, draining the wound. Pre-antibiotic time this is. That side of the family – fishermen in the Baltic for centuries – each and every one has at least one of these events during childhood or early adolescence. Every 50 birth or so a baby is born with turtle-like hands or hand and feet. Several hundred years ago rumor has it that a baby was born with a fishhead – sort of a Mgritte like creature I suppose, and they are supposed to have just tossed it into the sea. Because they are fishemen, are they regressing?

          • John Scanlon, FCD
            Posted April 24, 2013 at 1:05 pm | Permalink

            I think Günter Grass must have known some of your relatives.

            • truthspeaker
              Posted April 24, 2013 at 1:14 pm | Permalink

              I was going to go with HP Lovecraft but your literary joke is much less obvious and therefore funnier.

            • Posted April 24, 2013 at 7:32 pm | Permalink

              My relatives are from the western part of the Baltic, Grass and his Kashubian clan are from the area around Dansk/ Danzig. But Grass is great on matters like fishing, fish and the like. very earthy writer.

    • Posted April 20, 2013 at 8:46 am | Permalink

      The strictly anatomically correct term would be pharyngeal slit, although the term gill slit is often used. Gill slits (which strictly correctly occur only in fishes) and pharyngeal slits are homologous structures. Gills are the elaborated lamellar structures with a rich blood supply for respiration that are found within the slit. All chordates have pharyngeal slits, but not all chordates have gills.

      In explaining the condition to a patient, a physician might well use the more well-known term gill, and I see nothing terribly wrong with that. Should the patient inquire further, the physician could explain the nomenclatural, phylogenetic and anatomical details.

      Persistence of an open slit is a rare condition, and I’m intrigued that it seems to be heritable in your family. I’ve never seen someone with the condition, but a colleague had a student who had a persistent, unobtrusive slit into which she (the student) could insert a pencil!

      GCM

      • Posted April 20, 2013 at 9:21 am | Permalink

        The point is that the slit or gill wants to open up at a certain point,but cannot, and thus a cyste-like infection ensues. I’ll get in touch with the family and try to have the next incidence also regarded by a geneticist and have cell samples taken. The scar on the left side of my neck is about five inches long! And when asked about it in this country, since I first sat foot at the Brookln Pork of Embarkation, I used to say “from a rumble in Brooklyn.” The kids in highschool and college never disputed the possibility!

  3. Endre Kovács
    Posted April 19, 2013 at 5:48 pm | Permalink

    A Fish Caught in Time by Samantha Weinberg is a remarkable little book on the discovery of the coelacanth.

    • Mark Joseph
      Posted April 20, 2013 at 12:02 pm | Permalink

      I was also going to recommend that book. Great read.

  4. truthspeaker
    Posted April 19, 2013 at 6:02 pm | Permalink

    Very interesting.

  5. Posted April 19, 2013 at 6:20 pm | Permalink

    I know this is wildly off-topic, but how has no one here posted this, yet?

    http://www.ustream.tv/tinykittens

    Saw it over on Pharyngula! Though not posted by PZ… :D

  6. BilBy
    Posted April 19, 2013 at 7:00 pm | Permalink

    Larry Moran over on ‘Sandwalk’ has criticised this paper over the claim that ‘coelacanths evolve more slowly’: anyone who is more versed in genetics than I able to counter to weigh in?

    • Posted April 19, 2013 at 10:23 pm | Permalink

      All he says is he doesn’t believe it. That’s not a counter argument, that’s an a priori opinion. Variations in evolutionary rates between lineages are well documented, so I’m not sure why he objects to the claim it varies in coelacanths. It is of course possible that Amemiya et al. have made some error in their analysis, but you’d have to point out the error, or reanalyze their data and show the rate is typical (or even more rapid) to show that they are wrong.

      GCM

      • Posted April 20, 2013 at 2:17 am | Permalink

        I am in no way qualified to argue with Moran, but I got the impression that his objection is motivated by his own emphasis on drift, and justified only to the extent that the authors don’t make it clear that their remarks apply only to non-degenerate changes in coding DNA

        • Marcoli
          Posted April 20, 2013 at 6:20 am | Permalink

          That is also what I got out of the posting by Moran. The authors of the Nature paper conclude that coelacanth proteins have changed less than proteins in other vertebrates, but one can still expect that they do as much genetic drift as any group. I found it to be a good point. Also the authors describe the coelacanth as a ‘living fossil’, and that has become a criticized term right now. Not sure what the problem is with that.

          • Marcoli
            Posted April 20, 2013 at 6:31 am | Permalink

            If anyone wants to chime in about living fossils, they might do so near my entry about it a little farther down.

    • Torbjörn Larsson, OM
      Posted April 20, 2013 at 4:05 am | Permalink

      Presumably, if they have established a fair estimate of evolution rate, they may restore older estimates that seems criticized. Or at least that is what the Wikipedia coelacanth page claims, with a reference dated 2013:

      “In addition, it was shown recently that studies concluding that a slow rate of molecular evolution is linked to morphological conservatism in coelacanths are biased by the a priori hypothesis that these species are ‘living fossils’.[10]” [ http://en.wikipedia.org/wiki/Coelacanth ]

      On the other hand it could become an academic fight, Moran’s obsessions about genetic drift aside. [/takes out popcorn, looks at the package, puts it back for now]

  7. neil
    Posted April 19, 2013 at 8:57 pm | Permalink

    Coelacanth. The preferred fish of Blue Man Group.

  8. Torbjörn Larsson, OM
    Posted April 20, 2013 at 3:55 am | Permalink

    Thanks! A really nice counterpoint to the initial article, who all concentrated on the story device of ‘living fossil’ and how the halved evolutionary rate somehow supported that.

    Never mind that this clade has speciated recently (was it within the last 5 my, I can’t remember), or as their wiki page says “several recent studies have shown that coelacanth body shapes are much more diverse than is generally said”.

    I had forgotten about the urochordates. Having neural crest cells, and cephalochordates none? [Sez the squiddly one in -07.] Amazing!

    • Torbjörn Larsson, OM
      Posted April 20, 2013 at 4:08 am | Permalink

      I think my 1st correction experienced a javascript fail, it didn’t append.

      Another error, I meant “lineage”.

  9. Torbjörn Larsson, OM
    Posted April 20, 2013 at 3:56 am | Permalink

    Initial articles.

  10. Marcoli
    Posted April 20, 2013 at 6:29 am | Permalink

    So what is the problem with the term ‘living fossil’? Is that a valid reference to coelacanths and horseshoe crabs? I had been thinking about it lately, and right now I am coming down on it being still ‘OK’, but naive. If they are living fossils then so are cyanobacteria and many many other prokaryotes and a horde of protists and about 100,000 other species.

    • Posted April 20, 2013 at 8:12 am | Permalink

      You more or less have it correct Marcoli. “Living Fossil” implies that they have not changed; the opposition to using the term comes from realization that the similarity of extant forms to fossils is strictly superficial, and that a great deal of evolution has taken place but been concealed by those superficial similarities. Biologists pretty well understood this already, but the term is more confusing to lay-people, and so rife for abuse by YECs who want to exploit that confusion.

  11. jimroberts
    Posted April 20, 2013 at 6:38 am | Permalink

    sub

  12. Posted April 20, 2013 at 11:32 am | Permalink

    THE COELACANTH BY OGDEN NASH

    Consider now the Coelacanth
    Our only living fossil
    Persistent as the amaranth
    And status quo apostle
    It jeers at fish unfossilized
    As intellectual snobs elite;
    Old Coelacanth, so unrevised
    It doesn’t know it’s obsolete

    from Candy is Dandy p 374

    NEXT

    I thought that i would like to see
    The early world that used to be,
    that mastodonic mausoleum
    the Natural history museum
    At midnight in the vasty hall
    The fossils gathered for a ball
    High above notices and bulletins
    Loomed up the Mesozoic skeletons
    Aroused by who knows what elixirs
    The ground along like concrete mixers
    They bowed and scraped in reptile pleasure
    And then began to tread the measure
    There were no drums or saxaphones
    But just the clatter of their bones
    A rolling, rattling carefree circus
    of mammoth polkas and mazurkas
    Pterodactyls and brontosauruses
    sang ghostly prehistoric choruses
    amid the megalosauric wassail
    I caught the eye of one small fossil
    Cheer up old man, he said and winked
    It’s kind of fun to be extinct

  13. Sean
    Posted April 20, 2013 at 2:22 pm | Permalink

    My grandparents lived in East London(Eastern Cape Province btw) and I loved the trips to the Museum. I was fascinated by the story of the coelacanth, and sparked my love of natural history.

    I had understood it was important find when I was a kid but didn’t realize it was this significant.

    Thanks for the great website ! A pitty that wonderful scientists like Jerry C. Have to waste time fighting the religious to accept what should be common knowledge and can’t dedicate all there effort to their studies. How much further would we be ?

    Keep up the good fight on our behalf!

  14. Posted April 20, 2013 at 2:33 pm | Permalink

    Jerry et al., thanks for covering this story and for covering a previous one from my lab on programmed genome rearrangement in lampreys. Very much appreciated. There is some great discussion on the coelacanth here. Thanks all for your interest. Yes, the fin-limb story is what most folks think about when discussing the invasion of terra firma by fishapods… but that is clearly not the only thing of importance. The evolution of pharynx and all manner of physiological changes are also really important. We have our work cut out for us over the next few years.

  15. marksolock
    Posted April 20, 2013 at 8:37 pm | Permalink

    Reblogged this on Mark Solock Blog.

  16. microraptor
    Posted April 21, 2013 at 12:04 am | Permalink

    One thing that this has reminded me of:

    There’s the line about how the Coelacanth disappeared from the fossil record for 65 million years until the specimen was discovered in a fish market.

    So I’ve been wondering, modern Coelacanths are a deep-sea species. How good is the fossil record for deep sea organisms, anyway? It just seems like of all the various habitats on the planet, the deep sea would be the worst ones simply because most of the fossil beds for deep sea areas would still be in the ocean, away from where the fossils could really be found. Yes? No?

    • Notagod
      Posted April 21, 2013 at 10:17 am | Permalink

      I’m not enough of a geologist to answer except to note that some of the land that is now at a relatively high elevation was once under water. I expect that you already knew that but not sure if you considered it in this case. Now, where is the gravelinspector anyway?


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