Reinventing the worm


i-1bc8375bf73650319bed813cbac1e39a-buddenbrockia_sm.jpg

Sometimes, I confess, this whole common descent thing gets in the way and is really annoying. What we’ve learned over the years is that the evolution of life on earth is constrained by historical factors at every turn; every animal bears this wonderfully powerful toolbox of common developmental genes, inherited from pre-Cambrian ancestors, and it’s getting rather predictable that every time you open up some fundamental aspect of developmental pattern formation in a zebrafish, for instance, it is a modified echo of something we also see in a fruit fly. Sometimes you just want to see what evolution would do with a completely different starting point — if you could, as SJ Gould suggested, rewind the tape of life and let it play forward again, and see what novelties arose.

Take the worm. We take the generic worm for granted in biology: it’s a bilaterally symmetric muscular tube with a hydrostatic skeleton which propels itself through a medium with sinuous undulations, and with most of its sense organs concentrated in the forward end. The last common ancestor of all bilaterian animals was a worm, and we can see that ancestry in the organization of most animals today, even when it is obscured by odd little geegaws, like limbs and armor and regional specializations and various dangly spiky jointed bits. You’ll even see the argument made that that worm is the best of all possible simple forms, so it isn’t just an accident of history, it’s a morphological optimum.

But what if we could rewind the tape of life a little bit, to the first worms? Is it possible there are other ways such an animal could have been built? It seems nature may have carried out this little experiment for us, and we have an example of a reinvented worm, one not constructed by common descent from that initial triumphal exemplar in the pre-Cambrian — an alternative worm.

I’ve been waiting for this paper to come out since I first heard Peter Holland speak about at SICB. It’s a description of a worm, Buddenbrockia … but what a worm.

Buddenbrockia plumatellae is a parasite that lives inside bryozoans. It looks just like a tiny worm from the outside — it’s a slender tube — but on the inside and in its history it’s very different. Phylogenetic analyses show that this worm is most closely related to the Myxozoa.

Myxozoans are weird, weird, weird. Aquarists run into them all the time: they are responsible for whirling disease in fish, where this nasty parasitic myxozoan infests the brains of the animal and turns them into frantically spinning freaks until they die and release the spores of the parasite. They were thought to be protists for a long time, but then molecular work showed that they have various proteins associated only with metazoans, and they were then regarded as degenerate animals that had abandoned the joys of multicellularity to frolic as more simplified eukaryotes.

On the basis of the similarity of certain structures in the spores, the polar capsules, that resemble the nematocysts of cnidarians, they’re also thought to be, basically, greatly stripped down descendants of ancient jellyfish-like animals. This work from the Holland lab nails that down with a genomic analysis that aligns Buddenbrockia with the Myxozoa, and the Myxozoa with the Medusazoa. What this means is that a simplified lineage of cnidarians, radially symmetric diploblasts that do not look wormlike at all, which had degenerated into even greater simplicity to live as an aquatic parasite, has one descendant that has either retained a primitive structure or re-evolved some degree of multicellular complexity, and has independently evolved the worm. This animal is not descended from that bilaterian worm we take for granted, at any rate.

So it’s a worm of independent origin from all us other glorified worms. What’s different about it?

i-72b767f488e7bb8e3e512c37d9cbf058-buddenbrockia.jpg
A zooid of the bryozoan Plumatella
with Buddenbrockia worms (arrow) in the body cavity. Scale bar, 40 µm. (B) Cross section of an immature Buddenbrockia plumatellae worm. Note the presence of four longitudinal muscle blocks (M) and absence of gut. Scale bar, 20 µm. (C) Scanning electron microscopy image of a Buddenbrockia plumatellae worm. Scale bar, 100 µm.

First, the aspects that are the same are the external elongate appearance, an internal fluid-filled space that acts as a hydrostatic skeleton, and its ability to locomote with sinuous undulations. Those are properties that make it a worm in the first place.

The way it does that is different, though. There is no gut at all. This is an animal that lives off the nutrients from its host, in which it is awash. It has no sense organs and no recognizable nervous system — sinuous locomotion requires muscular coordination, though, so I assume motor control is through waves of electrical activity through the muscles themselves, or through epidermal connections. It also has an usual mode of locomotion, coiling like a spring and straightening, which may be a useful way of escaping from its host (a cnidarian version of Spring Surprise). It is not bilaterally symmetric: it has two axes of symmetry and four longitudinal bands of muscle, so it’s actually a tetraradial worm.

Many of the attributes of the animal, such as the lack of a gut or sense organs, aren’t particularly titillating, since they’re most likely a product of the parasitic lifestyle of the creature. Tetraradial symmetry provokes the imagination, though — what if our ancestor, the ancestor of most metazoan clades, had been a tetraradian rather than a bilaterian? Try to imagine if our familiar animal life had been built on a body plan with four-fold, rather than two-fold, symmetry. Reinventing animal life with just a subtle tweak like that at the root of the tree would have dramatic effects on all the subsequent branches. This is a most unprepossessing worm, but our distant ancestors were similarly humble — but the patterns of their genes echo and re-echo through all of us, and those early choices have shaped and constrained our evolution every step of the way.


Jiménez-Guri E, Phillipe H, Okamura B, Holland PWH (2007) Buddenbrockia is a cnidarian worm. Science 317:116-118.

Comments

  1. Apikoros says

    Very nice. Weird animals and a Python reference?

    I’m thrilled down to my dangly spiky jointed bits!

    Interesting about the tetraradial symmetry– does that mean that the longitudinal axis of this worm maps to the dorsal-ventral axis of its ancestors, like a jellyfish that got very tall?
    Does it have any specialized areas along its length?

  2. says

    But what if we could rewind the tape of life a little bit, to the first worms?

    Well, obviously we would find tape-worms.

    Bob

  3. Antti Rasinen says

    Shame they don’t have five-fold symmetry. Then they’d be like the Old Ones in Lovecraft’s At the Mountains of Madness. And that would be both creepy and cool at the same time.

  4. says

    I know spring is over and us Northern Hemispherians are well into summer, but did anyone else get a little flushed at “a bilaterally symmetric muscular tube with a hydrostatic skeleton which propels itself through a medium with sinuous undulations, and with most of its sense organs concentrated in the forward end”?

  5. says

    Oh, those poor tetraradial children, intellectually oriented and socially awkward, who go through their entire neoteny-prolonged larval stage hearing the taunting epithet, “Hey, eight-eyes!”

  6. mojojojo says

    A four-lobed brain! With one central corpus callosum, or four separate ones, or both?

  7. Todd says

    That is way cool. These guys would make perfect ID mascots because they’re brainless, gutless parasites.

  8. says

    If the sinusoidal movement is like that of a regular bilat worm/snake/fish, then it would be really interesting to find out whether the plane of that movement varies randomly (either locking in once it starts, or by some underlying physiology) or whether the coordination mechanism somehow gets locked to a particular plane. Of course, given the spring behavior, I have to wonder if the sinusoidal movement is helical instead of planar… I’ll have to see if I can get the real paper, but I thought I’d toss this out as food for thought…

  9. says

    Is there a relatively short, non-biologist comprehensible explanation about the evolution of the 5-based appendages in arthropods, echinoderms, mammals and whatever else?

  10. says

    Woah, PZ, that worm is a case analogous to the octopus brain! If we ever get to study extraterrestrial life, chances are we’ll find worms and beings with brains much like ours.

  11. Sven DiMilo says

    Very cool animal. No true gut, of course, but no gastrovascular cavity? no mouth/anus?

    I’m thinking that if you take something like Hydra, and have it take up an endoparasitic lifestyle, then feeding tentacles are useless and lost and you’re left with a simple hollow cylinder, more or less a “worm.” If absorptive nutrition throught the ectodermis works, then the the GV cavity closes up (as in tapeworms)and–bam! a cnidarian worm. Long-time lineages have had lots of time to explore bauplan-space, I guess.
    What’s really fascinating is the (presumed) continued simplification in some lineages to give secondarily unicellular myxozoans. So cool.

    IIRC, there are molluscan worms as well.

  12. David Marjanović says

    Medusazoa

    Medusozoa.

    it has two axes of symmetry

    Two planes, actually… :-}

    Is there a relatively short, non-biologist comprehensible explanation about the evolution of the 5-based appendages in arthropods, echinoderms, mammals and whatever else?

    What do you mean by 5-based?

    Myxozoans, BTW, are not really unicellular. The spores have something like 4 cells (including the two “polar capsules”) with complicated cell-cell adhesion, and the feeding stage is a plasmodium (a huge cell with huge numbers of nuclei).

  13. David Marjanović says

    Medusazoa

    Medusozoa.

    it has two axes of symmetry

    Two planes, actually… :-}

    Is there a relatively short, non-biologist comprehensible explanation about the evolution of the 5-based appendages in arthropods, echinoderms, mammals and whatever else?

    What do you mean by 5-based?

    Myxozoans, BTW, are not really unicellular. The spores have something like 4 cells (including the two “polar capsules”) with complicated cell-cell adhesion, and the feeding stage is a plasmodium (a huge cell with huge numbers of nuclei).

  14. says

    Mojojojo, you owe me another can of Pepsi. the last one is now on the lab floor where i almost gave myself another hernia laughing at Furries for Christ.

    Lepht

  15. says

    What do you mean by 5-based?

    5 digits on each limb (for a very large percentage of mammals, although it’s not obvious in some)

    5 limbs/sections (most echinoderms)

    5 limbs per side (spiders, crustaceans, etc.)

  16. Rupert Goodwins says

    Ah, thanks for that. This is exactly the sort of thing I love Pharyng for – the sort of insight that makes me go ‘if I had my time over again, then I’d like to have done this’ (no, not degenerate into a gutless parasite – I’m already in the media – but be part of a revolution in our understanding of life).

    Rupert

  17. Sven DiMilo says

    “Myxozoans, BTW, are not really unicellular. The spores have something like 4 cells (including the two “polar capsules”) with complicated cell-cell adhesion, and the feeding stage is a plasmodium (a huge cell with huge numbers of nuclei).

    Thanks for the clarification. Equally cool that way.

  18. Encolpius says

    It’s a little known fact that you can get a myxozoan to go away by tricking him into saying his name backwards.

  19. David Marjanović says

    5 digits on each limb

    Eh, that’s a reduction. Originally there were more: 6 (Tulerpeton), 7 (hindlimbs of Ichthyostega), 8 (forelimbs of Acanthostega). S. J. Gould used that as a book title: “Like the Hand’s Eight Fingers”.

    5 limbs/sections

    Echinoderms are five-sided the way we are two-sided. “Pentameric radial symmetry”.

    5 limbs per side (spiders, crustaceans, etc.)

    You only counted the biggest ones of the crustaceans — except the first antennae — and forgot the chelicerae of the spiders. The original arthropod condition is a limb pair per segment, and way more than 5 segments.

    So, I think all those occurrences of the number 5 are coincidence.

    It’s a little known fact that you can get a myxozoan to go away by tricking him into saying his name backwards.

    LOL!!!

  20. David Marjanović says

    5 digits on each limb

    Eh, that’s a reduction. Originally there were more: 6 (Tulerpeton), 7 (hindlimbs of Ichthyostega), 8 (forelimbs of Acanthostega). S. J. Gould used that as a book title: “Like the Hand’s Eight Fingers”.

    5 limbs/sections

    Echinoderms are five-sided the way we are two-sided. “Pentameric radial symmetry”.

    5 limbs per side (spiders, crustaceans, etc.)

    You only counted the biggest ones of the crustaceans — except the first antennae — and forgot the chelicerae of the spiders. The original arthropod condition is a limb pair per segment, and way more than 5 segments.

    So, I think all those occurrences of the number 5 are coincidence.

    It’s a little known fact that you can get a myxozoan to go away by tricking him into saying his name backwards.

    LOL!!!

  21. Kseniya says

    And it’s no coincidence that there are 10 letters in “Sven DiMilo”, is it, now?

  22. Kseniya says

    (Is it just me, or has anyone else noticed a chronic lack of Creo postings on threads like this?)

  23. Scott says

    quibble:

    Historical constraints are overrated. History influences subsequent evolution, but I think that it is an overstatement to say that it CONSTRAINS it. If there is strong enough selection, organisms can and do evolve away from their starting minima in any direction. Given enough time, every lineage end up being so different from its ancestors as to have almost erased all traces of homology. Really the only characteristics of lie that have been retained (i.e., are constraints) are nucleic acids and other basic mechanisms immediately linked to the most fundamental aspects of cell-level fitness.

  24. metzgerm says

    Are there any examples of land animals with greater than bilateral symmetry?

    If not, why not, since they seem to do well in oceans? Just thinking that if we did have four arms we would have more problems than just less elbow room–it really would constrain complex body plans in a way that might have made it impossible for any tetraradial animals to spread across land without first loosing the extra symmetry. But I never get to play with anything bigger than viruses and tissue culture, so I have no idea.

  25. says

    Before anyone reads any weirdass numerology onto my question, I was curious why we evolved into 5’s as opposed to 8’s or 4’s or 7’s, or 312’s. I wasn’t expecting that there was some flower-power cosmic significance to it. I just wondered if the 5’s were related somehow.

    So, I think all those occurrences of the number 5 are coincidence.

    That works.

  26. says

    Quoth Encolpius: “It’s a little known fact that you can get a myxozoan to go away by tricking him into saying his name backwards.”
    True — but the bugger will come back in 90 days…

  27. says

    Are there any examples of land animals with greater than bilateral symmetry?

    If not, why not, since they seem to do well in oceans?

    Warning: I’m making this up as i go along, so I can’t guarantee it’ll make sense.

    In answer to the first question, none that I can think of. In answer to the second – good question. Bilateral symmetry seems to be involved with evolution of an anterior-posterior axis, which seems a common consequence of high mobility – but then, echinoderms can be relatively mobile. Echinoderms also mess up the other point I had, which is that increased mobility and hence bilateral symmetry allows an animal to become an active hunter of food rather than a passive hunter or filter-feeder (Note – I’m using ‘hunter’ fairly loosely here to indicate an animal that actively looks for its food, rather than waiting for the food to come to it). Filter-feeding doesn’t work in a terrestrial environment – compared to in the water, the air just doesn’t carry enough nutrients. That’s why, for instance, while there are plenty of terrestrial gastropods, there are no terrestrial bivalves. On the other hand, echinoderms may be a special case of phylogenetic contingency, being seemingly derived from filter-feeding ancestors (which modern-day crinoids still are). You may wonder why can’t there be a omnidirectional hunter, which is what echinoderms essentially are? It may be because encephalisation (the development of a head) allows for a greater concentration of more developed sense organs in one place, as well as potentially a more developed brain, which is more effective than a diffuse network. Echinoderms only have the latter.

    In terms of a longitudinal animal with radially spaced appendages, maybe there’s an efficiency factor in this too. Many tube-dwelling and burrowing worm-like animals have this sort of arrangement, but once an animal adopts a vagile lifestyle and probably a preferred dorsal and ventral side, the dorsal appendages become much more redundant, with most manipulation, support, etc. roles going to the ventral appendages. And there are probably advantages to having the mouth displaced ventrally rather than pointing directly forward – it allows for easier approach to food, easier manipulation of food by bringing it closer to the ventral appendages, greater ability to guard food items from competitors and/or watch for predators while eating…

    Buddenbrockia intrigues me on this front, actually, as I see relatively little reason for it to be worm-like. It doesn’t need to move anywhere – it sounds like its movements with the host coelom are pretty much random. Sven DiMilo is probably right in that the basic worm-like shape may just be a result of the loss of cnidarian tentacles and gut, but then why the well-developed muscle blocks? Offhand, the presence of muscle blocks in itself isn’t that unusual – the Jiménez-Guri et al. paper cites their presence in other cnidarians (an anemone, IIRC), while muscle blocks are also present in ctenophores, which molecular data suggest may be more distant from bilaterians than cnidarians are.

    Whew, that was nearly a post in itself.

  28. Peter Ashby says

    Thankyou PZ so much for posting that, I am enthralled. How btw did you manage not to express your desire to see a cleavage stage embryo? How do you build a creature with two axes of symmmetry? Something to chew one for quite a while.

  29. Peter Ashby says

    Scott, Firstly we are patently constrained by history. Just you try and get from mammalian eyes to cephalopod ones. It is patently obviously better not to have a blind spot, no saccades, no brain mechanism so the organism fails to notice them etc. As for our origins being subsumed, that is what developmental biology is FOR, to lay them bare again. Are we protostomes or deuterstomes? look in the embryos. Do we have a dorsal or ventral nerve cord? look in the embryos (adults are no good, they twist and stuff). Why do we have neuronal cell death? what a waste, those constraints again. I can think of a dozen weird ways of doing things in development that only make sense in the light of constraints. It must be energetically beneficial to get rid of cell death. It is clearly possible to grow extensions (limbs, tails) so why are digits formed in a plate and only defined by the cell death of the tissue between them? so you can make ducks? no, because our ancestors had fins.

  30. Azkyroth says

    metzgerm and Christopher Taylor:

    Intriguing. Since I’m at least idly an aspiring science fiction author these sort of thoughts are useful…incidentally, I actually designed an amphibious sentient race a few years back that were secondarily bilateral, evolved from ancestors with three-lobed radial symmetry. Maybe it’s time to revive them… ^.^

  31. jotetamu says

    David at #25:
    Gould’s book is “Eight little piggies” in English. You must be thinking of the French edition, “Comme les huit doigts de la main”.

    Jim Roberts

  32. says

    It seems to me that this is a pretty good response to Conway Morris’s criticism of Gould in “Crucible of Creation”. He seemed to say that replaying life’s tape would have turned out about the same, partly because of convergence and partly because (he claimed) that the apparent peculiarities of the Burgess Shale creatures were just superficial, and that their deep structure was probably not as unusual as their appearance. This organism seems to be convergently somewhat similiar to worms, but quite different at the deep level.

    Here’s my favorite faux worm — a caecilid amphibian.

  33. says

    Here’s my favorite faux worm — a caecilid amphibian.

    Well, there goes my lunchbreak.

    My favorite discovery from this bit of impromptu research:

    The hatchlings of the oviparous East African Boulengerula taitanus have special teeth that allow them to peel and eat their mother’s skin. The mother’s skin in this species was found to be thicker than normal and contained a high level of fat and other nutrients.

  34. Twirlip Of The Mists says

    Is there a relatively short, non-biologist comprehensible explanation about the evolution of the 5-based appendages in arthropods, echinoderms, mammals and whatever else?

    This would be due to interference from the hexapodia conspirators, who seek to reduce future competition.

  35. David Marjanović says

    Gould’s book is “Eight little piggies” in English. You must be thinking of the French edition, “Comme les huit doigts de la main”.

    Maybe it’s the UK title then (US and UK editions often don’t share a title). You’re right about the French version, but I’m pretty sure I’ve seen in English, too.

    —————–

    Yes, caecilians are awesome. So are amphisbaenians. Mwahah.

  36. David Marjanović says

    Gould’s book is “Eight little piggies” in English. You must be thinking of the French edition, “Comme les huit doigts de la main”.

    Maybe it’s the UK title then (US and UK editions often don’t share a title). You’re right about the French version, but I’m pretty sure I’ve seen in English, too.

    —————–

    Yes, caecilians are awesome. So are amphisbaenians. Mwahah.

  37. says

    Filter-feeding doesn’t work in a terrestrial environment – compared to in the water, the air just doesn’t carry enough nutrients.

    Also, getting back to the structuralism discussion, the physical constraints on land due to gravity are different than they are in water. Aquatic animals develop and navigate in 3D space as easily as we do in 2D–we can move anterior-posterior or left-right very easily, but when we go up-down, we have to either fight gravity or control it from taking us down too fast. So perhaps buoyancy mitigating the effects of gravity, and the concomitant effects on available motion, play some kind of role in the development of axes of symmetry as well.

    Azkyroth, it is interesting to speculate what the atmospheric properties of that world would be that such a species would be well-suited for.

  38. says

    Maybe it’s the UK title then (US and UK editions often don’t share a title).

    hee-hee. As an Agatha Christie fan since childhood, I can think of some totally inappropriate examples of *that* phenomenon.

    Nowadays, though, it’s probably less about racism and classism, and more that focus groups in the UK test differently than their counterparts in the US.

  39. Scott says

    Peter, I understand that history influences subsequent evolution, but I still object to the idea of constraints. Of course evolution tinkers with what already exists in the face of new selective pressures, but I would argue that a real constraint can only be identified by leading to extinction. Otherwise, the selective pressure was addressed in a satisfactory way, who cares if it is optimal – it is good enough. There isn’t selection to become optimal. Who cares if digits are produced in a fashion that requires apoptosis … so evolution tinkered with an ancestrally lobed fin rather than inventing digits de novo. It was good enough to do it this way, and even if we might look at is suboptimal, clearly we would be wrong. It is very effective to make digits this way. Has been for a long time, probably will be for a long time.

    “Constraint” implies that something cannot evolve (to my mind at least; maybe I’m being too strict). I don’t think we are qualified to determine what cannot evolve. Whales are arguably suboptimally adapted to life in the ocean becuase they still have to breath air. Does that mean that they will always have to breath air. I doubt it, there is surely a way around it. Its just that right now that is good enough. But if it stops being good enough, they will either evolve towards a different strategy or go extint. Perhaps examples of true constraints could be found by looking at organisms that did go extinct. Even so, maybe they just didn’t get lucky enough to evolve how they needed to, even though it was possible.

    I have more thoughts on the issue, but lunch calls….

    Scott