Pharyngula

Where do the hagfish fit in?

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Hagfish are wonderful, beautiful, interesting animals. They are particularly attractive to evolutionary biologists because they have some very suggestive features that look primitive: they have no jaws, and they have no pectoral girdle or paired pectoral fins. They have very poorly developed eyes, no epiphysis, and only one semicircular canal; lampreys, while also lacking jaws, at least have good eyes and two semicircular canals. How hagfish fit into the evolutionary tree is still an open question, however.

There is a strong temptation to see hagfish as representing an earlier grade of evolution than the lamprey, regarding them as a sister group to the vertebrates, with a tree like this:

i-06f1aad74a12ae8cec54b59f76334d78-hagfish_sister.jpg
If the hagfish is regarded as a sister group of
the vertebrates, Conel’s description of an “epithelial crest”
appears to be an intermediate state of the fully evolved crest,
which delaminates to produce migrating crest cells, as seen in
vertebrate embryos including lamprey embryos.

The primitive features of the hagfish represent a contemporary retention of the ancestral state. One of the key pieces of evidence for this version is the development of the neural crest, illustrated in green on the right. The neural crest is a highly plastic population of migratory cells that arise at the time of the closure of the neural tube; in vertebrates, these arise by delamination, or separation of the cells, from a dorsal epithelium. Earlier reports of neural crest in hagfish suggested that they arose in that animal as epithelial pockets, a very different approach, and that the evolution of the neural crest was from an initial state of a set-aside epithelial tissue.

I described some other work on the evolution of vertebrate eyes in which the authors make an argument this sister state of the hagfish is valid, and that therefore the time of divergence of the hagfish represents a lower bound on the period when eyes evolved. Hagfish don’t have image-forming eyes at all; lampreys have good image-forming eyes; if the tree diagram above is correct, we can narrow down the period of eye evolution to the time between the branching of the hagfish line and the divergence between lampreys and the gnathostomes, or jawed vertebrates. Cool.

There’s an alternative picture, though. Hagfish could be degenerate forms: the jawless fish, lampreys and hagfish, form a monophyletic group, and the hagfish secondarily lost their eyes. In this model, they really don’t tell us much at all about the ancestral state, because their morphological simplifications are not primitive at all — they’re more recently evolved specializations.

If this is the case, than the tree should be redrawn like this, to illustrate cyclostome monophyly.

i-6e7d2438ce89589e1a9ea8ff37751333-cyclo_monophyly.jpg
Monophyly of the Cyclostomata is consistent with the
actual development of the hagfish crest and with the recent
observation of presumed “neural-crest-like cells” in ascidian
embryos.

This is an active debate right now. As I mentioned, one side is testing hypotheses by looking at the details of cellular organization and molecular pathways—if the hagfish has molecular relics of a more complex ancestral visual system, for instance, that would reinforce the idea of cyclostome monophyly. I’ve also reported that hagfish eggs and embryos have finally been successfully raised in the lab, and the results so far are that they don’t have an unusual mode of neural crest formation at all — previous interpretations otherwise were the result of fixation artifacts, and hagfish seem to make neural crest by delamination, just like everyone else. There is also a growing body of molecular information that’s tying hagfish and lampreys closer together.

Personally, I think the argument for cyclostome monophyly is growing stronger, while those who think hagfish are a more primitive sister group seem to be fighting a rising tide of evidence. Still, this is how scientific debates are settled: by testing hypotheses and gathering evidence. We follow where the data leads.

OK, that’s all very rarefied and academic, but here’s another reason hagfish are just plain interesting: they’re weird, and they do many things in such a different way than we vertebrates with our faces and our jaws are used to imaging them. Here, for example are a few frames from a video sequence showing how an alien eats a piece of meat.

i-cbd3ba5ad1cdf255f90bee869662df59-hagfish_feeding.jpg
Successive video images of the moment of feeding. The fish protrudes a pair
of plate-like “horny teeth” (tp) ventrally to capture the bait (cod meat). Also note the tentacle surrounding the dorsal “nostril” (no) and the
ventral “mouth” (mo).

Spectacular!


Kuratani S, Ota KG (2008) Hagfish (Cyclostomata,
Vertebrata): searching for the ancestral developmental plan of vertebrates. BioEssays 30:167-172.

Comments

  1. #1 MAJeff
    January 15, 2008

    “Cool.”

    Yup.

  2. #2 True Bob
    January 15, 2008

    hagfish fit in the much needed niche habitat for slime producers

  3. #3 Cameron
    January 15, 2008
  4. #4 gg
    January 15, 2008

    Hmm… I have a feeling that a giant version of one of these puppies might destroy NYC on the 18th… :P

  5. #5 Rey Fox
    January 15, 2008

    The Creeping Terror! Whatever you do, don’t crawl into its mouth!

  6. #6 Mrs Tilton
    January 15, 2008

    they have no jaws, and they have no pectoral girdle or paired pectoral fins. They have very poorly developed eyes, no epiphysis, and only one semicircular canal

    That’s as may be, but nothing can beat them at goobering up great gouts of snot.

  7. #7 Stanton
    January 15, 2008

    In a previous blog entry about them, didn’t you mention that this one group of students discover that hagfish slime makes for a good egg-substitute?

  8. #8 True Bob
    January 15, 2008

    …hagfish slime makes for a good egg-substitute?

    Ummm, for vandalism, maybe. Who’s gonna be the first to try the hagfish snot omelet?

  9. #9 Brownian, OM
    January 15, 2008

    We really should be more conscientious about using the term ‘basal’ rather than ‘primitive’, given the tendency for non-biologists (and a few biologists as well) to misunderstand the meaning of the latter.

  10. #10 beardedbeard
    January 15, 2008

    Thanks PZ, next time someone tells me we should teach the controversy I am going to ask them what side of the great Hagfish debate they are on.

  11. #11 DaveX
    January 15, 2008

    Brownian– Since you mentioned it, I’ll have a little “basal” in my hagfish snot-omelet. Some onion would also be nice.

  12. #12 Brownian, OM
    January 15, 2008

    You know, I feel like an omelette. You think I could have a hagfish omelette with shallots, but with the shallots only slightly browned…?

  13. #13 Cyde Weys
    January 15, 2008

    Creepy looking things. But judging by the environment they live in (and them being scavengers rather than predators, presumably?), it does make sense that eyes and jaws could degenerate for them, the same way eyes of cave fish do. Some ignoramuses will claim that this is devolution, but of course it isn’t; why grow eyes when, on the balance, the energy put into growing them isn’t repaid? Eyes aren’t free, and if you don’t use them enough, might as well not have them. Plus, it’s much easier for evolution to disable features (it could be as simple as a single SNP) than to recreate them from scratch.

  14. #14 Sven DiMIlo
    January 15, 2008

    Coupla good hagfish-slime vids:

    http://www.youtube.com/watch?v=Bb2EOP3ohnE

    and

    http://www.youtube.com/watch?v=NYRr_MrjebA
    (slime at about 3:45)

  15. #15 Sven DiMIlo
    January 15, 2008

    Well, cyclostome monophyly is not quite as good a story, but oh well. Even if hags & lampreys are each others’ closest living relatives, the split was a looooooong time ago.

  16. #16 True Bob
    January 15, 2008

    I’ll have the Hagfish Snotomelet, spam, toast, juice, spam and spam.

  17. #17 True Bob
    January 15, 2008

    I’ll have the Hagfish Snotomelet, spam, toast, juice, spam and spam.

  18. #18 K. Signal Eingang
    January 15, 2008

    …sushi eating sushi. Yow.

  19. #19 Greg Peterson
    January 15, 2008

    Speaking of vision and degeneration, with apologies if this has been covered and I missed it, but I thought this research was very cool as well:

    Progeny of blind cavefish can regain their sight
    Blind cavefish whose eyes have withered while living in complete darkness over the course of evolutionary time can be made to see again, according to a report in the January 8th Current Biology, a publication of Cell Press. In some cases, the offspring of mated pairs originating from distinct cave populations regain vision, they found. The result shows that mutations in different genes are responsible for eye loss in separate cavefish lineages that may not have been exposed to light for the last one million years.

    “Restoration of the ability to see comes in a single generation because the populations residing in different caves are blind for different reasons–i.e., different sets of genes are non-functional in the different populations,” said Richard Borowsky of New York University. “[In the hybrids], the deficiencies in one lineage are compensated for by the good gene copies in the other lineage, and vice versa.”

    Scientists know of twenty-nine populations of the blind cavefish (Astyanax mexicanus) living in different caves in North-Eastern Mexico, he said. They evolved from eyed, surface-dwelling forms which only reached the area in the mid-Pleistocene, about a million years ago.

    Earlier studies found that the evolutionary impairment of eye development — as well as the loss of pigmentation and other cave-related changes — results from mutations at multiple gene sites, or loci. Reports also showed that eye loss has evolved independently at least three times and that at least some of the genes involved differ between the different cave populations.

    “Given the large number of mutations at different loci that have accumulated in these populations, we reasoned that hybridization among independently evolved populations might restore visual function,” Borowsky said.

    And indeed, it did. While purebred cavefish are all blind, the hybrid progeny of different cave populations all had some individuals that exhibited a clear visual response. The farther apart the caves of the cavefish parents were, the more likely it was that their offspring could see, he added. That pattern is consistent with the idea that populations separated by greater distances are more distantly related and therefore have less overlap in the genes responsible for their blindness, he said.

    In addition to the insights about the evolution of cavefish in particular, the findings also speak to a more general principle. “Evolution’s palette is varied,” Borowsky said. “There are numerous genetic ways to accomplish the same change.”

  20. #20 Noadi
    January 15, 2008

    The scary thing is the hagfish snot is probably more nutritious than the spam.

    I like to think of myself as being adventurous when it comes to trying new foods but whoever was the first person to try hagfish snot has my complete respect because I couldn’t do it.

  21. #21 John Emerson
    January 15, 2008

    At my URL is my hagfish page. It’s a joke page, but some of the links are interesting. One describes the use of hagfish slime in place of eggwhite for baking.

    Hagfish are a food fish in Korea, and a lot of the fish leather you see is hagfish leather.

  22. #22 bernarda
    January 15, 2008

    Undoubtedly many people will contact you about Colbert’s interview with Neil Shubin. But, just to speed things up.

    http://onegoodmove.org/1gm/

  23. #23 Rey Fox
    January 15, 2008
  24. #24 David Marjanovi?, OM
    January 15, 2008

    We really should be more conscientious about using the term ‘basal’ rather than ‘primitive’, given the tendency for non-biologists (and a few biologists as well) to misunderstand the meaning of the latter.

    Be very careful about that, though, because it doesn’t mean the same thing. If anything, “basal” means “furthest away from the group I’m most interested in right now”. For examples, there are papers on the phylogenetic position of the turtles that say the mammals are the basalmost amniotes, and they’re right from their perspective.

  25. #25 David Marjanovi?, OM
    January 15, 2008

    We really should be more conscientious about using the term ‘basal’ rather than ‘primitive’, given the tendency for non-biologists (and a few biologists as well) to misunderstand the meaning of the latter.

    Be very careful about that, though, because it doesn’t mean the same thing. If anything, “basal” means “furthest away from the group I’m most interested in right now”. For examples, there are papers on the phylogenetic position of the turtles that say the mammals are the basalmost amniotes, and they’re right from their perspective.

  26. #26 David Marjanovi?, OM
    January 15, 2008

    (Of course, that’s a single example…)

  27. #27 David Marjanovi?, OM
    January 15, 2008

    (Of course, that’s a single example…)

  28. #28 Matt H
    January 15, 2008

    Really liked the point in the article where PZ wrote that

    In this model, they really don’t tell us much at all about the ancestral state, because their morphological simplifications are not primitive at all — they’re more recently evolved specializations.

    The idea that morphological simplification represents specialization is probably a GREAT way to answer IDiots. Think about it – they rant (quite incorrectly) that evolution defies the second law of thermodynamics because things get more complex….but they don’t, always. Forms adapt to the environment over generations.

    Clearly this is another reason to assign students to program Life….they might understand how an organism adapts to the conditions it finds itself in. Of course, some student complain that cellular automata don’t represent actual life; that’s when the words analogue and model come out.

    Sigh.

  29. #29 Sven DiMilo
    January 15, 2008

    David’s right, but Brownian’s larger point is also correct: there is really no good use for the term “primitive” in modern biology. Traits can be “ancestral” or “derived;” whole animals are what they are.

  30. #30 Moses
    January 15, 2008

    hagfish fit in the much needed niche habitat for slime producers

    Posted by: True Bob | January 15, 2008 1:59 PM

    Benny Hinn.

  31. #31 Hank Fox
    January 15, 2008

    Sorry, I can’t see them as beautiful. When I look at those pictures of feeding, I keep imagining Karl Rove dropping his expandable jaw to eat a live rat, like Diana from “V.”

  32. #32 Brownian, OM
    January 15, 2008

    If anything, “basal” means “furthest away from the group I’m most interested in right now”.

    Hmm, I figured as much. That’s unfortunate, since in non-biological contexts ‘basal’ means at the base or stem, or can refer to something foundational or base.

    Well, whatever is used in phylogenetics to mean less-derived or retaining-more-characteristics-of-a-common-ancestor, we should be using that, or be satisfied that there will always be a sizeable component of the population that wonder how an extant species can be considered more ‘primitive’ than another extant species when evolution has always and continues to act on them both.

  33. #33 Brownian, OM
    January 15, 2008

    Ooh, ‘ancestral’! That’s what I meant.

    Thanks David and Sven. I’ve only a passing understanding of cladistics (and the complexities of that field which do not often lend themselves to simple explanations readily understood by those outside it) and I find it fascinating. I think it would do a lot for the general understanding of biology if it were given a more thorough treatment than it currently is at the high school level.

  34. #34 Bureaucratus Minimis
    January 15, 2008

    We really should be more conscientious about using the term ‘basal’ rather than ‘primitive’, given the tendency for non-biologists (and a few biologists as well) to misunderstand the meaning of the latter.

    By all means use whatever term is most appropriate when writing journal articles. But please remember us struggling laypeople when writing for a more general audience. SJ Gould struck a good balance with this, yet I constantly referred to my dictionary when reading Wonderful Life.

    When I read “primitive” in this context, I think of a (relatively) simple organism that has been around for a long time, with relatively minor changes.

  35. #35 Todd
    January 15, 2008

    Brownian, I checked out your blog and you don’t look like an omellete.

    I’m not familiar with Hagfish but they seem very well adapted to deep water scavenger feeding; streamlined to get inside carrion easily, very slow metabolisms, able to go long periods without food, etc.

    According to Wikipedia they are technically invertebrates since they don’t have spines but do have cartilaginous skulls. Did they lose their spines as well as their eyes or have they never had vertebra?

  36. #36 Jim Thomerson
    January 15, 2008

    Terms we are needing here are plesiomorphous (basal, primative, whatever) and apomorphous (advanced, etc.) Symplesiomorphies are shared primative characters which tell us nothing about relationship. Synapomorphies are homologies which inform us as to relationships.

  37. #37 Sven DiMilo
    January 15, 2008

    Good question, Todd. The old story was B, never had em, so the name Craniata was invented for the group including hagfish + “True vertebrates” (was it Romer who wrote that hagfish are considered vertebrates as a courtesy only, or something like that?). If cyclostomes are, in fact, monophyletic though, that would seem to suggest loss of vertebrae in hagfish. Like I said above, not as good a story.

  38. #38 Stanton
    January 15, 2008

    I’m thinking that they never had true vertebrae is the main reason why hagfish are considered “invertebrates”

  39. #39 j.c
    January 15, 2008

    hagfish are also usefull for making wallets there was a commercial fishery for them here in washington a few years ago but no one could stand handling the slimy things

  40. #40 Dave Godfrey
    January 15, 2008

    I’m still not convinced about hagfish & lamprey monophyly. This is mostly because when you add fossils lampreys usually nest with various anaspids, jawless fishes much closer to the gnathostomes, whereas hagfishes almost always end up at the base of the tree. The number of reversals that seem to be required for this doesn’t seem parsimonious. Nor does the alternative (lots of convergence in lampreys).

    Part of the problem is probably because all we have left of the agnathans are two not particularly diverse groups of rather specialised animals both of which are significantly different from anything you might use as an outgroup, that long-branch attraction is going to be a big problem.

  41. #41 nn
    January 15, 2008

    Re #36: sounds like hagfish slime is an excellent adaption
    (or better exaption) against humans then. A lot of other fish would be lucky if they had something similar. Unfortunately it doesn’t work
    in Korea.

  42. #42 Diego
    January 15, 2008

    We might have come full circle, pardon the pun, with the cyclostome, eh? I remember that when I was an undergrad our survey course taught that hagfish and lamprey were joined in the Agnatha. It was out-of-date taxonomy in the late 90s and was one of many relics of a course that had not been updated in a while. Even then I was reading on my own that hagfish had been moved to the sister group of the vertebrates. And now we’re going back to clustering the two together. Of course we’re only talking about the crown group agnathans (Agnatha is still paraphyletic and won’t make a return), but it’s interesting to see that the consensus about these two clades is swinging back.

  43. #43 Sven DiMilo
    January 15, 2008

    Thanks, Dave Godfrey (#37)…it’s good to know there’s yet hope for the better story. As for symplesiomorphies and synapomorphies, I find “shared ancestral characteristics” and “shared dewrived characteristics,” respectively, to be much easier to understand and remember!

  44. #44 mothra
    January 15, 2008

    Cladist terminology here is plesiomorphic or apomorphic meaning ancestral and derived traits, respectively. If the derived traits are found in a single species, the term is Autapomorphic. If many taxa share a derived trait it is a Synapomorphic trait. The term ‘symplesiomorphic’ is really a misnomer and yields no information as the traits involved are not ‘shared’ in the sense of the prefix ‘syn/m’ unless we are discussing the level in a hierarchical classification at which the traits are, in fact, synapomorphies. Example: Except for a few creos, posters at this site are cellular organisms. From our viewpoint, cellularity would be symplesiomorphic- but at the level where cellularity is useful in classification, the Eukaryotes, it is a synapomorphy because it then denotes a holophyletic group.

  45. #45 J. Grybowski
    January 15, 2008

    …sushi eating sushi. Yow.

    As a current resident of Japan, I am afraid I must protest this bit of ignorance. Strange though Japanese tastes in marine life may be, raw fish does not constitute “sushi” as such. It is vinegared rice, with or without an exotic sea creature on top, which makes up the “sushi”. Truly, “sushi eating sushi” would be a nigh-miraculous feat of Oryza cannibalism.

    …Though I admit that I have sometimes wondered whether a few of the things I’ve eaten here were not alive when I did so.

  46. #46 truth machine
    January 15, 2008

    That’s as may be, but nothing can beat them at goobering up great gouts of snot.

    Put it in a pretty bottle with flowers on it and you could sell it as a personal lubricant.

  47. #47 Alan Kellogg
    January 15, 2008

    I have to wonder about hagfish and lamprey teeth. Those strange conodont like assemblages of calcium phosphate that help the animal grind up food.

    Proposition: Hagfish and lampreys form a clade related to, but not directly part of, the vertebrates. The two clades forming the Vertebrataformes.

  48. #48 sublunary
    January 15, 2008

    I was amused to notice that the ad for next week’s episode of Dirty Jobs shows Mike on fishing for “slime eels”. Just as I was wondering if that’s another term for hagfish, they show a picture of him, holding one and looking disgusted.

    I can’t help wondering if the hagfish fishermen will tell us about the egginess of their slime…

  49. #49 Ba'al
    January 15, 2008

    People tend to forget that the normal vertebrate state is THREE eyes — the two lateral ones people normally think about, and the pineal body, which is very retina-like in pretty much every vertebrate lineage except mammals (where the pineal is comparatively degenerate). The morphological development of pineal (and the genes that control it, e.g. Pax6) is quite similar to lateral eyes. Personally, I find the absence of a hagfish pineal body (epiphysis) at all stages compared to the very elaborate one of lampreys to argue against monophylety. Even a larval lamprey has a well developed pineal body, even though its lateral eyes are poorly developed and are more like hagfish. In my mind this argues against the idea that the the lateral eyes of hagfish represent a neotenous state.

  50. #50 C. Sullivan
    January 15, 2008

    I seem to be in the minority here, but I actually think “primitive” is a perfectly good, intuitively straightforward term for a basal group that also retains a lot of plesiomorphic features. A group alive at the present time can still be primitive if it didn’t accumulate many autapomorphies on its journey to the present. Hagfish would qualify as primitive under phylogeny “B” (actually the one that comes first on the page) but not under phylogeny “A”.

  51. #51 PZ Myers
    January 15, 2008

    Yeah, I’m afraid that in anything written for a general audience, the arcana of cladistics terminology is the kiss of death. I think it’s a good thing to use terms that don’t bear the value-laden implications of words like “primitive”, but it’s hard to balance comprehensibility with accuracy.

  52. #52 Niel D
    January 16, 2008

    K.Signal Eingang said:
    “…sushi eating sushi. Yow.”

    Actually, I think you’ll find that’s “sashimi”. Sushi is rice prepared with vinegar.

    http://en.wikipedia.org/wiki/Sushi

  53. #53 Nigel D
    January 16, 2008

    D’oh! What a stupid place for a typo!! Comment #49 was me.

    C. Sullivan –

    There is a genuine objection to the use of the term “primitive”, because it implies that there is some kind of progression from “primitive” to “advanced” in extant organisms. Whereas, in truth, all extant organisms have been evolving for the same length of time.

    Thus, the terms “ancestral” and “derived” are preferred, because they are more precise and do not carry that connotation.

  54. #54 Brownian, OM
    January 16, 2008

    Ah, I see. Nigel D is the more derived form of Niel D.

  55. #55 Peter Ashby
    January 16, 2008

    The problem with your argument about the pineal Baal is the first part of it provides the answer for the second. If the genetic mechanisms for pineal formation are the same as for lateral eyes then if primitive eyes are degenerate in hagfish then the genetic mechanism by which this happened could also have done for the pineal. It obviously must work fairly early in development, or degenerate pineal is hard to see or recognise in the embryos. If as PZ says we have only just got a handle on breeding them in the lab complete absence of the pineal in embryos must be up for revision surely.

  56. #56 Liesele
    January 16, 2008

    um…#14…just out of curiosity what constitutes a GOOD hagfish-slime video? ‘Cause I’m just saying, um, ew. From a scientific standpoint, of course.
    Just joking people. I’m actually the type who looks at biological oddities (from our point of view) and says, “cool!”

  57. #57 A farinosa
    January 16, 2008

    I can’t say hagfish slime omelets would be any more objectionable than bird’s nest soup (swiftlet snot). Hagfish do make for better wallets than swiftlets.

  58. #58 Mark Powell
    January 16, 2008

    Hagfish conservation is now a necessity, believe it or not. So-called “slime eels” are a target since cod and other more desirable species in deep decline. Save the hagfish.

  59. #59 Jim Thomerson
    January 16, 2008

    Many years ago, when the world was young, I attended a seminar on the pituitary. There were slides shown of fossil skulls (amphibian maybe?) which had, not three, but four eye sockets. It may have been suggested that their pituitary eyes were actually image forming.

  60. #60 sgp
    January 17, 2008

    Although hagfishes and lampreys ARE intereseting, the most interesting thing about the cladogram to me
    is the relative position of tunicates and lancelets.
    What work provides the evidence that tunicates rather
    than lancelets are the sister-group to the the vertebrates?

    Anyone know the nature of the morphological/molecular bases for such reasoning?

    As for primitive/basal, one should always use care to use such terms only in the context of particular characteristics and a particular model of phylogeny (hypothetical tree topology).

    If they taste anything like raw lancelets forget it. As for sashimi, don’t forget the wasabi, if you add enough wasabi one could eat raw Myxine and not even know it.

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