Hagfish embryos!


i-7e80ff6ee77c160f6ca547f5ef88f958-hagfish_egg.jpg
A hagfish egg with a 14.3-mm pharyngula-stage embryo inside (arrows). Scale bar, 5 mm.

I’ve been looking forward to seeing these little jewels in print since I saw Kuratani talk about them at the SICB meetings in January. Hagfish are wonderfully slimy jawless chordates that have been difficult to raise in the lab—although if you poke a whale corpse rotting in the cold deeps you’ll find them swarming everywhere. The Kuratani lab has managed to keep animals of the species Eptatretus burgeri alive and healthy in a lab aquarium maintained at cold temperatures (16°C), and has even had success in breeding them. That object to the right is a single hagfish egg, brown and leathery-shelled and surprisingly big—it’s an inch and a half long!

They collected 92 eggs, and then another limitation emerged: it took 5-7 months for embryos to develop in a small number of the eggs. Hagfish aren’t going to be your typical fast-developing model system, I’m afraid, but they are extraordinarily cool animals, and it’s good to see work beginning on them.

So what do the embryos look like? To no one’s surprise, much like your typical chordate embryo—note the pharyngula stage embryo in d and f, with the divisions of the brain visible, and distinct eyes and ears. It’s beautiful.

i-78a0581cbc1c384f751e605b4fa80864-hagfish_embryo.jpg
c, A 7.4-mm embryo, corresponding to the late neurula stage. d, A 14.3-mm embryo, corresponding to the early pharyngula stage. e, The head of the 7.4-mm embryo. f, The head of the 14.3-mm embryo. fb, forebrain; hb, hindbrain; mb, midbrain; ot, otic pit; ph, pharyngeal wall; som, somites; TC, trigeminal crest cells. Scale bars, 5 mm (cd); 1 mm (e, f).

One reason to be interested in hagfish embryos is to resolve questions about the origin of specific chordate evolutionary novelties. They are more primitive than lampreys in many ways, and in particular, we’d like to know more about a specific embryonic tissue, the neural crest, in these animals. The neural crest was a key innovation that was crucial in providing the raw material for much of the vertebrate head.

Previous studies of hagfish embryos (from 1899! It’s been a while) relied on small numbers of embryos that were typically poorly fixed — note the large yolky eggs, which are always problematic. Those studies suggested some unusual mechanisms of neural crest generation in the hagfish.

i-0e982eb8b567fcbe90d614cbc0d335c4-hagfish_phylo.gif
a, The hagfish may be either the sister group of all the other vertebrates (1), or that of lampreys (2). b, c, Hypotheses on neural crest evolution. b, The former hypothesis (1) would agree with the scenario that neural crest evolution had an intermediate epithelial state. c, Alternatively, the crest might have already been established as a population of delaminating cells in the common ancestor to all vertebrates, and this would be coherent with both hypotheses (1 or 2).

The neural crest arises from a population of cells that are produced at the boundary of the neural tube and epidermis during neurulation. In familiar vertebrates, the neural crest cells delaminate or peel away from the top of the nervous system and migrate as a loose mass called mesenchyme to new destinations in the body. The early descriptions of the hagfish suggested something different: instead of delaminating, the sheet of cells that gives rise to the epidermis and neural tube retains coherence instead of delaminating, and folds into little pouches that run the length of the body (the dark loops in b, above). If true, that would be curious and different, and would suggest that perhaps neural crest first originated as an epithelium, rather than a mesenchymal mass.

Kuratami’s work suggests that the earlier interpretation was wrong, and was an artifact produced by poor fixation. They’ve now examined embryos that are well fixed, and have also been able to stain the tissue with modern probes specific for neural crest and other neural markers. The answer is that hagfish neural crest emerges like that of other chordates, as a loose collection of cells that migrates preferentially in the spaces between the somites.

i-75904a38c8e4b8b7e1c9a235f3d768cd-hagfish_crest.jpg
Putative neural crest cells in a 7.4 mm hagfish embryo. b, Illustration of neural crest cell distribution in the embryo on the basis of three-dimensional reconstruction from the histological sections; seen from the anterior oblique view. Red arrows indicate the ventrally migrating crest cells occurring at the same intervals as the apices of somites shown by purple circles. c, Schematic representation of a horizontal section of the embryo to show the planes of sections d and e. d, A transverse section at the mid-somite level. No putative crest cells are found between the somite (som) and the neural tube (nt). Asterisks in c and d indicate the apex of each somite. e, A transverse section at the intersomitic level. Putative crest cells (arrowheads) are filling in a space between the somite and the neural tube. n, notochord; nt, neural tube; som, somite. Scale bars, 100 µm.

These are useful results — they push back the origin of important embryological features to the common ancestor of hagfish, lampreys, and gnathostomes, and suggests that they may have appeared over 500 million years ago. These animals are going to be important intermediates to study, although the difficulty and slow rate of development is rather daunting. Maybe we need to get some fanatical aquarists working on more efficient aquaculture methods — wouldn’t you love to have a tank full of hagfish to play with in your home?


Ota KG, Kuraku S, Kuratani S (2007) Hagfish embryology with reference to the evolution of the neural crest. Nature 446:672-675.

Comments

  1. Dark Matter says

    Dr. Myers-

    What is the function of the filaments at the poles of the egg in
    the first picture? Are they for respiration or for attachment to tissue?

  2. says

    They didn’t say. Respiration seems unlikely, though — they’re just too small to make a significant difference.

  3. Inky says

    This is great; a few weeks ago a speaker and I were talking about hagfish and we were wondering what their embryos looked like. They’re gorgeous.

    Not like the adults, who are unequivocally pinky ugly.

  4. says

    Yes I would love an aquarium full of hagfish. This is really exciting stuff on so many levels. So much to learn on everything from evo-devo to behavior.

    makes me wish I hadn’t segued out of biology into IT.

  5. Curt Cameron says

    Natasha wrote:
    Yes I would love an aquarium full of hagfish.

    I don’t think you’d want an aquarium full of hagfish, or even with one hagfish, at least if it was your job to keep that aquarium clean.

  6. TheBlackCat says

    I agree with Curt. From what I read a single hagfish can turn a bucket of water into a bucket of slime in a matter of minutes.

    Wikipedia says that tufts are for making the eggs cling to one another.

  7. wright says

    Great stuff; my compliments to the Kuratani lab staff for their hard work. The ecology and biology of the deep ocean is one of the great frontiers of science. Nice to see that being pushed back a bit.

  8. David Livesay says

    “Cool”? A lot of adjectives come to mind when I think of hagfishes, but “cool” isn’t one of them. They’ve got to be about the most disgusting living things. The ability to secrete a bucketful of mucus in seconds flat isn’t my idea of cool. It’s just gross.

    By the way, did anybody catch Kings of Camouflage on Nova the other night? Now those things are cool!

  9. Goby says

    “What is the function of the filaments at the poles of the egg in
    the first picture?”

    Some goby eggs have filaments on one end for attachment to the substrate so that the eggs do not drift away on the currents. This could be a possible function for the filaments on the hagfish eggs.

  10. David Livesay says

    What is the function of the filaments at the poles of the egg in
    the first picture? Are they for respiration or for attachment to tissue?

    Just a wild guess here, but they look somewhat reminiscent of the filaments at the ends of some elasmobranch egg cases. These are coiled to wrap around stems of underwater macrophytes. The ones on the hagfish egg don’t have this structure, but if we knew what kind of substrate they’re usually deposited on, it might explain how they work.

  11. tinisoli says

    Hagfish are nightmarish. They come up in the body cavities of cod and other fish snagged in gillnets, and they spill out on the deck, wriggling and purple and far more frightening than anything else I ever saw while observing fisheries. There’s actually a fishery for hagfish. Barrels are sent to the seafloor, and the hagfish swim inside through small holes, go to work on the bait within, and then get hauled up. The meat and skin is valuable in South Korea, I’ve heard.
    I used to tell my mom that if I died before my parents I wanted them to feed me to the sharks. I’m not sure I feel as cavalier about being fed to hagfish.

  12. says

    As ugly as adult hagfish may be, they’re the main constituent part in most “eelskin” wallets.

    Look, it’s commerce in embryo form!

  13. Ray says

    Someone from Minnesota thinks 16 degrees Celsius is cold (about 60 degrees F)? PZ, your love of hagfish is making you soft.

  14. buglady says

    I hate to be such an old poop, but whenever I see cool comparative research being done on a somewhat difficult model system, I can’t help but notice that it almost never originates from a lab in the US. The funding system here just won’t support the extra effort, instead focusing on more rapid and assured payoffs. I’m glad that other countries aren’t so short-sighted.

  15. kat says

    Ray, I think he was suggesting 16 C was cold compared to the temperatures most developmental biologists working with fish are used to. Zebrafish (being tropical fish) are kept at a significantly higher temperature – around 25-27 C, or 76-80 F.

    It’d be interesting to know how much of the difference in developmental speed can be explained by the temperature difference alone. I know I’ve seen (maybe from the moens lab?) a chart showing the development rate of zebrafish embryos at different temperatures… they can be manipulated to some extent. It’d be interesting to see if hagfish embryos could develop at higher temperatures, or if they have to remain within a narrow range.

  16. says

    You can find that data in the zebrafish staging series. Yes, most of us aquarists are used to tropical fish and keeping heaters on our tanks to make them happy; 16°C is cold water. Letting my fish drop down to 20°C would be debilitating and lethal.

  17. Scott says

    So, here we have a really “primative looking” creature. Yet, this creature has been evolving as long as we have. So what do we think happened? Are they just so very well adapted to their environmental nitch that have had no need to change? But even random mutations happen now and then. Do we think they have changed? If they really haven’t changed in tens of millions of years, there’s got to be some strong selective pressure to maintain their present form. That’s a more amazing concept than the speed with which other species evolve.

    Any thoughts on how species like the hag fish don’t evolve?

    Thanks for the always fascinating posts.

  18. amph says

    Great post on a great paper. Where can I buy hagfish?
    Easy predictions:
    (1) Since this paper is in part a correction on earlier (19th century!) work, some creationist sect will come with a statement that “Darwinists had to admit that contrary to what was previously thought,.. [fill in some silly interpretation]..”. Somehow the statement will look to naïve eyes as if Kuratani has actually confirmed Genesis.
    (2) PZ and a number of other bloggers, with foam on their mouths, will tear that account apart and we will all have something to laugh about.
    (3) One more time we have to clean our monitors or keyboards.
    (4) Nothing is ever heard anymore on this subject from the creationists; they are not even interested–their job was finished after (1).

  19. CCP says

    We used to get a few live hagfish as demonstration material for an organismal biology course I TAed a million times…Man it was fun to grab one, let it slither out of your hand, and hold up a gooey handful of agnathan snot.
    (pedantry re PZM’s comment #23: “You can find that THOSE data…” Come on, people, we have to hold the line on this one!)

  20. CCP says

    (pedantry re PZM’s comment #23: “You can find that THOSE data…” Come on, people, we have to hold the line on this one!)
    preview…preview…preview…

  21. Darby says

    I don’t know about hagfish, but other long-stable forms often have extremely efficient DNA repair and proofreading mechanisms (that’s part of the reason why sharks rarely get cancer). They’ve evolved to not evolve.

  22. Coragyps says

    I think I remember that hagfish slime is unslimy until it hits seawater, and then a teaspoonful gives a gallon of snot. We use a great deal of similar-looking snot to pump down oil wells – so get a big aquarium started, and we’ll sell all the waste at a profit!

  23. Nick Gotts says

    Is it true they are the only animals that are known to be able to tie themselves in a knot? Or could some of the cephalopods manage this?