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« Hard to disbelieve | Main | Oh, the ignominy of it all »

We have the brains of worms

Category: DevelopmentEvolutionMolecular BiologyOrganismsScience
Posted on: May 4, 2007 12:45 PM, by PZ Myers

Way back in the early 19th century, Geoffroy St. Hilaire argued for a radical idea, that vertebrates and most invertebrates were inverted copies of each other. Vertebrates have a dorsal nerve cord and ventral heart, while an insect has a ventral nerve cord and dorsal heart. Could it be that there was a common plan, and that one difference is simply that one is upside down relative to the other? It was an interesting idea, but it didn't hold up at the time; critics could just enumerate the multitude of differences observable between arthropods and vertebrates and drown out an apparent similarity in a flood of documented differences. Picking out a few superficial similarities and proposing that something just looks like it ought to be so is not a persuasive argument in science.

Something has changed in the almost 200 years since Geoffroy made his suggestion, though: there has been a new flood of molecular data that shows that Geoffroy was right. We're finding that all animals seem to use the same early molecular signals to define the orientation of the body axis, and that the dorsal-ventral axis is defined by a molecule in the Bmp (Bone Morphogenetic Protein) family. In vertebrates, Bmp is high in concentration along the ventral side of the embryo, opposite the developing nervous system. In arthropods, Bmp (the homolog in insects is called decapentaplegic, or dpp) is high on the dorsal side, which is still opposite the nervous system. At this point, the question of whether the dorsal-ventral axis of the vertebrate and invertebrate body plans have a common origin and whether one is inverted relative to the other has been settled, and the answer is yes.

That raises more questions, of course. One is where the nervous system fits into this scheme. Flipping upside down would seem to be a fairly radical change in organization, and it's difficult to imagine (failures of our imagination are not scientific data, of course, but trying to reconcile conceptual difficulties can lead to new ideas) how inverting everything could be accomplished while still retaining viability. One resolution of that problem that has been proposed is to simplify: maybe the last common ancestor of arthropods and vertebrates was dorso-ventrally ambiguous — it was a worm for which up and down didn't really matter, making it easy for one branch of its descendants to commit to one orientation, while another branch committed to the reverse orientation. The key to this idea was the suggestion that maybe that last common ancestor didn't have a central nervous system — it had a distributed nerve net, and only after the vertebrate lineage had separated from the others did the central nervous system (CNS) condense on the side opposite Bmp's expression. In this case, the CNS of vertebrates and invertebrates would not be homologous; they would have arisen independently. I've discussed this idea before, in the context of hemichordate evolution.

One way to resolve the question of whether the CNS is homologous across the metazoa would be to look for more details; the more similarities we can accumulate in the molecular patterning of the nervous system, the less likely they are to be of independent origin. I also reported on some work in Drosophila that showed similarities in how the fly and vertebrate nervous system are patterned — within the CNS, we all use Bmp to generate a gradient that defines zones where particular neuron types differentiate. These data made it increasingly improbable that the metazoan CNS evolved multiple times, but these competing hypotheses of a patterned CNS in the bilaterian last common ancestor vs. no CNS in the LCA and independent origin are still duking it out. I am amused to quote myself; I ended that article on fly CNS patterning with a question:

The way to resolve this is, of course, more comparative data. How are the Bmps used in the Lophotrochozoa?

I am amused because I just got my hands on a paper from the Arendt lab that describes Bmps and CNS patterning in the Lophotrochozoa. If it weren't such an obvious question to have asked, I'd call myself a prophet.

Here's an overview of the situation in vertebrates. The neural tube is patterned by a double gradient: Bmp is high dorsally and low ventrally, while Sonic hedgehog (Shh) is high ventrally and low dorsally. Cells in the CNS can read their position in the gradient, and that defines their identity and their properties as neurons. It's a system that sets up columns of cells in the neural tube with similar functions. For instance, there is a longitudinal column of motor neurons, neurons that will reach out to innervate muscles, near the floor of the tube all along its length.

neurulation3.jpg

What the Bmp/Shh double gradient does is activate different transcription factors at different dorsal/ventral levels of the CNS. We can map those out, as diagrammed below.

cns_gradient.jpg

What you can see is that the gradient of Shh regulates other, downstream transcription factors. Where Shh is high, Nox6.1 and Nox2.2 are active; where Shh is low, Pax7 and Pax6 are active, and so on. Each dorso-ventral layer of the CNS has its own combinatorial code derived from the pattern of transcription factors operating in it.

That map of transcription factor activation sketches out the basic layout of the neural columns in the CNS. It's fundamental. There are many, many details that get added on top of it, of course, but it really represents a kind of primal framework, the skeleton on which the later, greater elaborations are built.

The paper from the Arendt lab examines these same transcription factors in a polychaete worm, Platynereis (I've discussed that worm before, too— it has very cool eyes). There's a huge amount of very impressive work in that paper — maps of gene expression, experimental manipulation of the Bmp gradient, staining for specific neurotransmitters, etc. — but I'm going to skip it all and jump ahead to the summary diagram. This is amazing. Look at the simpler diagram above; the one below is laid out in roughly the same way, with bars that stretch from the top of the diagram (dorsal in the vertebrate, lateral in the worm) to the bottom (ventral in the vertebrate, medial in the worm), with the domains of expression of various factors indicated by the extent of the bars. The vertebrate pattern is on the right, the worm pattern on the left.

platy_genes.jpg
(click for larger image)

Mediolateral Arrangement of Neurogenic Domains and of Neuron Types in the Annelid and Vertebrate Trunk Nervous Systems. The mediolateral extent of the expression of neural specification genes is represented by vertical bars. Dashed lines separate neurogenic domains with a distinct combination of neural specification genes. Colored bars represent the expression regions of neuronal specification genes at predifferentiation stages. Hatched bars represent genes that are expressed at differentiation stages only.

Whoa. There are obvious differences, but the most striking fact of the two diagrams is their general similarity. Lophotrochozoans and chordates clearly exhibit homologous patterns of organization in their earliest stages. The color coding in this diagram pushes the homology still further; it illustrates the function and transmitter types common in those domains, and they line up fairly well, too.

This next diagram illustrates the position of these transcription factors a little more concretely, in an outline of a cross section of the animal. One thing to keep in mind is the topological arrangement of the neural tube in vertebrates. Our nervous systems fold themselves over and tuck themselves into the body wall in a process called neurulation. The similarities are more obvious if you mentally unfold the vertebrate neural tube, flattening it out into a flat sheet so the red area is at the dorsal midline, and the purple dots are moved out laterally. Then it becomes obvious that the vertebrate is an upside-down copy of Platynereis.

platy_cns.jpg
(click for larger image)

(B) Comparison of mediolateral patterning in Platynereis, vertebrates, Drosophila and enteropneust. The schematic drawings represent trunk cross-sections of embryos. The medio-lateral extent of expression is shown for nk2.2 (red), pax6 (gray), and msx (cyan). Midline cells (black), serotonergic neurons (yellow), hb9+ neurons (blue), and ath+ lateral sensory neurons (purple) are indicated as circles.

What the presence of such similar mechanisms of neural tube patterning in vertebrates and polychaete worms suggests is that the last common ancestor of these two deeply divergent lineages, the Urbilaterian, also had a nervous system with a similar columnar organization of its CNS. Drosophila, which has a roughly similar pattern with some simplifications and differences, is the product of fairly extensive evolutionary changes; it's less primitive in its structure, and more derived. Similarly, other deuterostomes like the enteropneust in the diagram, have also thrown away most of the structure in their nervous systems, and their diffuse, nerve-net style architecture is not primitive either, but derived.

We're still left with the curious problem of how and why our ancient chordate answer flipped itself upside down and took to swimming about with its former belly upwards. The authors conclude with some speculation based on Dohrn's annelid theory; perhaps there was a semi-sessile stage in chordate history, where the animal was living partially buried in the substrate, basically lying on its back in the mud, filter feeding. When they made the transition to free-swimming, they simply retained their orientation and made other adaptations to effectively invert themselves, primarily in constructing a new ventral mouth.


Denes AS, Jekely G, Steinmetz PR, Raible F, Snyman H, Prud'homme B, Ferrier DE, Balavoine G, Arendt D (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129(2):27

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Comments

#1

Posted by: James Bremner | May 4, 2007 12:52 PM

Thats a mighty tasty apple. Thanks PZ

#2

Posted by: Garrett | May 4, 2007 1:01 PM

I'm still giggling about the signaling protein called Sonic hedgehog. I am, apparently, 8 years old.

#3

Posted by: K. Signal Eingang | May 4, 2007 1:17 PM

SCIENCE!

Fascinating read, and I think I may actually have understood most of it! Can't wait to regale all my friends with the state of the art in invertebrate neuro-embryology. I am going to be such a hit at my next cocktail party, I bet.

#4

Posted by: Mike Fox | May 4, 2007 1:28 PM

Are they thinking that the "living partially buried in the substrate, basically lying on its back in the mud, filter feeding" stage was the sea squirt / lancelet stages? Or before? Or after?

#5

Posted by: Paguroidea | May 4, 2007 1:43 PM

Yum!Yum! That apple was very delicious indeed.

#6

Posted by: Stuart Coleman | May 4, 2007 1:45 PM

Every question answered breeds yet more that need to be addressed. Hooray science!

#7

Posted by: Mike Crichton | May 4, 2007 2:01 PM

"See, you just ADMITTED that Athiestic Science was _wrong_ about something for 200 years! That means you're wrong about Evil-ution now!" There, I just saved the trolls some effort... ;-)

#8

Posted by: CCP | May 4, 2007 2:04 PM

I'm feeling pretty proud of myself for beating PZM to this one...I showed (& explained) those same diagrams to my Bio 102 class last Thursday! (perfect timing with the whole deuterostome/protostome thing)

#9

Posted by: Eamon Knight | May 4, 2007 2:07 PM

Are they thinking that the "living partially buried in the substrate, basically lying on its back in the mud, filter feeding" stage was the sea squirt / lancelet stages? Or before? Or after?

That would be the politician stage.

#10

Posted by: Ritchie Annand | May 4, 2007 2:32 PM

The way to resolve this is, of course, more comparative data. How are the Bmps used in the Lophotrochozoa? If it weren't such an obvious question to have asked, I'd call myself a prophet.

I remember once upon a time an English teacher raking me over the coals for daring to use qualifiers on the word "obvious". "It's either obvious or it's not," he'd say.

I still feel that he was wrong, in light of such usage :)

This stuff is neat. I had read in a few articles the vertebrate/invertebrate inversion, and I'm pleased to see how thoroughly evident this is the more we look.

Have any more biological prophecies for the coming decade? :)

#11

Posted by: The Physicist | May 4, 2007 3:02 PM

Interesting. Made me think about differences in nervous system. I was wondering if they can tell if bugs feel pain like we do? As a child I was pretty mean to bugs. Magnifying glass and grasshoppers in ant beds and garden spider webs.

#12

Posted by: Nick (Matzke) | May 4, 2007 3:19 PM

Apparently pelagic trilobites swam "upside down" so such things are not so inconceivable:
http://www.trilobites.info/trends.htm

I also recommend this "down with phyla!" post from PT on how simple twisting of the mouth in worms can produce "super-phylum"-level changes:
http://www.pandasthumb.org/archives/2005/04/down_with_phyla_1.html

#13

Posted by: mothra | May 4, 2007 3:19 PM

Pardon the pun but this may shed some light on the 'problem' with the vertebrate eye- blood supply between the retina and the incoming light source. WE then would be the group that 'flipped' and, the ecdysozoan bauplan might be closer to the pleisiomorphic condition for animal optical systems.

#14

Posted by: Steviepinhead | May 4, 2007 3:43 PM

Juat an excellent frickin' science post, PZ.

Thanks! I can tell you're already off to a great summer!

#15

Posted by: RogerQ | May 4, 2007 5:08 PM

Probably a silly question, but how does this "flipping upside-down" relate to the blastopore becoming the mouth in protostomes vs. the anus in deuterostomes? Is(n't) it the same thing? It seems to me that if you reverse which end is the mouth, you're essentially flipping which side is dorsal.

Imagine a protostome gastrula and a deuterostome gastrula, each oriented with the blastopore on the right. In this orientation, the nerve cord of both would form on the top (or bottom, take your pick). Then, to orient both creatures with their mouths to the left, you rotate the protostome 180 deg. on the z-axis (rotating the protostome on the y-axis, would change the left-right body-mapping in relation to the deuterostome). Now the nerve cord that was on the top in the protostome is on the bottom -- dorsal becomes ventral.

If this holds, then the same area of cells becomes the nerve cord in both protostomes and deuterostomes; which cells become the mouth (and eventually the head) is different.

Does this make any sense, or do I have my head up my blastula?

#16

Posted by: Mark | May 4, 2007 5:13 PM

I am immeasurably disappointed that you have a post involving invertebrate nervous systems without mentioning cephalopods. Have these systems been studied in cephs? Arthropods and worms are interesting, of course, but the ceph nervous system is an invertebrate system that probably also diverged from the arthropods and our common worm ancestor sometime in the Cambrian or earlier, and the ceph brain is considerably more centralized than most arthropods, so looking at the developmental control of cephalopod brain development might easily yield clues about whether, for example, the ceph vertical lobes share some developmental mechanisms with the hippocampus in vertebrates (since both are related to memory) or if the ceph visual lobes share any developmental systems with visual cortex (or area MT, or whatever) in vertebrates. I believe it's known that PAX6 is involved in the eye in cephs as well as arthropods and vertebrates, even though the development is somewhat different (see http://www.genome.org/cgi/content/full/14/8/1555 for example.)

If the eye development has surprising similarities in terms of gene expression during development, it seems like a no-brainer[sic] to compare the genetics of brain development of cephs to see if the advanced functions are tied back to that common-ancestor-worm somehow, or if cephalopods' advanced nervous system are fully the result of convergent evolution from a very primitive ancestor.

But noooo, you get all "grimpoteuthis is cuter than pokemonsters," but when it comes down to including cephs in your hardcore science, you drop the ball. Feh.

#17

Posted by: PZ Myers | May 4, 2007 5:16 PM

No, that's reasonable. The idea with the reversal is that chordates had to have evolved a new mouth.

What we need next is a few papers describing developmental mechanisms of oral specification in deuterostomes and protostomes.

#18

Posted by: PZ Myers | May 4, 2007 5:28 PM

Man, some people won't be satisfied with anything.

#19

Posted by: David Marjanović | May 4, 2007 5:37 PM

I still don't buy it.

The homologies are undeniable, but the inversion is IMHO not. I thought flatworms had no less than 8 nerve cords, dorsal and ventral and lateral? Why can't this be the ancestral condition? Has anyone checked if flatworms express BMP/DPP between their nerve cords?

(The mollusks would then have retained the ventral half of this arrangement: they have 4 nerve cords, all ventral. Hey! I mentioned cephalopods! :o) )

Also, RogerQ, if you have your head up your blastopore, that means you have a quite horrible case of spina bifida. In AFAIK all chordates, the caudal neuropore (hopefully) closes above the blastopore; we have both a stomodaeum (newly formed mouth) and a proctodaeum -- like the arthropods.

In arthropods, gastrulation happens on the ventral side and produces a midgut that is blind at both ends; then the blastopore closes while the midgut connects at the ends to invaginations from the ectoderm -- the foregut and the hindgut are ectodermal and even lined with cuticle.

Pardon the pun but this may shed some light on the 'problem' with the vertebrate eye- blood supply between the retina and the incoming light source. WE then would be the group that 'flipped' and, the ecdysozoan bauplan might be closer to the pleisiomorphic condition for animal optical systems.

Camera eyes are clearly not homologous between vertebrates and cephalopods -- the other mollusks and the other deuterostomes lack them. The comparison you need to make is AFAIK between the eyes and the pineal/parietal organs of vertebrates.

#20

Posted by: PZ Myers | May 4, 2007 5:49 PM

Hemichordates also lack the tidy discrete CNS.

The catch described here is that polychaete worms and chordates have very similar patterning mechanisms operating in their nerve cords. We have a couple of options.

a) the patterning of chordate/polychaetes is the ancestral state, and the hemichordates are derived and simplified.

b) chordates and polychaetes are not phylogenetically distant from each other, and we need to do some radical reorganization of the metazoan clades.

c) There has been an absolutely amazing amount of convergent evolution going on, and I have to go kiss and make up with Conway Morris.


(a) seems like the simplest and most likely answer to me.

#21

Posted by: lannejhang | May 4, 2007 6:04 PM

@PZ: Have a look at Arendt D. et al., Nature 2001: Evolution of the bilaterian foregut.
There are no developmental mechanisms in, but it adresses the point about the homology of the mouth in protostome and deuterostome larvae.

And as people are discussing about the development of the blastopore and its relation to the dorso-ventral axis, the same guy has also published something on this some time ago:
Arendt D & Nubler-Jung (Mech. Dev., 1997): Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates

#22

Posted by: lowk | May 4, 2007 8:01 PM

A post to print out and re-read before my "Genes, Genomes and Animal Evolution" exam, I feel.

#23

Posted by: Lowk | May 4, 2007 8:02 PM

(That was meant to come across more as "Thanks for the inspiring biology!" and less "Watch me steal your bio-fu!")

#24

Posted by: bad Jim | May 5, 2007 4:11 AM

Tunicates, anyone? We have sessile ancestral relatives. Doesn't anyone remember the old joke?

The juvenile sea squirt wanders through the sea searching for a suitable rock or hunk of coral to cling to and make its home for life. For this task it's equipped with a rudimentary nervous system. When it finds its spot and takes root, it doesn't need its brain any more, so it eats it.


It's rather like getting tenure.

#25

Posted by: Alan Kellogg | May 5, 2007 11:03 AM

What about planaria?

#26

Posted by: Dave K. | May 5, 2007 12:22 PM

Mark, your whining is getting really old. If you're going to bitch so much, why don't you start a better blog than Pharyngula?

#27

Posted by: PZ Myers | May 5, 2007 12:43 PM

Ummm...I don't see much evidence of "whining" in his record of comments. This one, yeah, a little bit too excessive in the fault-finding (this post wasn't about cephalopods!), but that hasn't been his history here.

#28

Posted by: Chasey | May 5, 2007 12:57 PM

madam fathom just posted on this too, and goes into a slightly different hypothesis as to how the inversion occurred (more similar to that proposed by Dohrn).

#29

Posted by: Chasey | May 5, 2007 2:17 PM

also, just a comment: if ANYONE had tried to publish this quality of work, with their in situ "double labeling," in an organism like zebrafish, it would have been SHOT. DOWN. Not to mention they did their Bmp experiments by putting Bmp proteins in the sea water "media," which I have never heard of doing. I didn't even know Bmps were soluble. In fact, I know this paper got terrible reviews (as did his last Nature paper), but one reviewer just happened to think it was a sexy story and deemed it worthy. My friend worked in the same lab as Detlev when the latter was a post-doc, in a zebrafish lab, and Detlev was the only scientist working on this worm. So while the rest of the lab was performing all these functional assays and working their asses off, Detlev does a bunch of in situs and gets a Nature paper. Bunch of in situs and gets a Cell paper.

Anyways. I believe the story, I'm just a bitter zebrafish scientist. :)

#30

Posted by: Drhoz! | May 5, 2007 9:42 PM

LOL at the tunicate joke.

then of course, there's the hermaphroditic flatworms, where there is a vas deferens between the male and female gonads :D

#31

Posted by: kobeboy | May 6, 2007 5:15 AM

RogerQ: re. blastopore, a earlier commentor mentioned the reveiw from Arendt and Nubler-Jung in 1997. This really is a good piece to explore those ideas (even though it was written 10 years ago). It may not completely add up (for example the blastopore of deutrostomes has an inductive action that has not been explored in protostomes). It's worth adding that assymmetries of particular genes (I'm thinking of dpp/bmp and sog/chordin) involved in DV axes exsist in cnidarians as well, although the realtionship between this axis and the bilaterian axes is fuzzy.

Chasey: Speaking as a scientist who does many functional assays day in and day out, I'm completely cool with a Cell or Nature paper that is "a bunch of in situs". They are incredibly informative in situs. Also BMPs are soluble, perhaps you're thinking of wnt/wingless or hedgehogs, which may act as lipocomplexes. Anyway this experiment was obviously a "figure 7" (for those wondering what a figure 7 is, the sticky wicket colomn in JCS once introduced this concept. It's a figure that is perhaps the weakest, least informative, experiment in a paper and is put there on the behest of a reviewer).

Anyway I don't think Arendt has unequivocally shown that we are upside-down worms, but it's nice data, and a good guide to others doing similar work. And when those other papers come along giving comparative embryologists a bonanza of data i think we'll get a good picture of how axes have evolved.

#32

Posted by: RavenT | May 6, 2007 6:26 AM

there's the hermaphroditic flatworms, where there is a vas deferens between the male and female gonads

Drhoz!, you leave me prostate from ROTFLMAO!

#33

Posted by: x_y_u | May 6, 2007 10:39 AM

@Chasey:
Cell does not publish papers just because one out of 3-4 referees think it's a sexy story, so I'm sure you know none of the referees' comments. And in any case you should know that referee comments are to be kept confidential. And stop spreading stupid nonsense about things you hear from your envious friend who didnt manage to get a Nature paper in his former lab. You didnt even get the fish species right your friend was working on...was not zebrafish but medaka.
It seems you both make a good team of frustrated scientists who might "work their ass off", but maybe don't have the brains to do the right experiments on the right species no matter what the techniques are.

#34

Posted by: David Marjanović | May 6, 2007 7:19 PM

Hemichordates also lack the tidy discrete CNS.

My point was that the flatworms have a neat, discrete CNS, with 8 cords instead of 4 or 2 or 1, so that we are probably looking at independent simplifications from that. Am I wrong about that?

#35

Posted by: George | May 7, 2007 10:05 PM

Me in student mode:
Question? In the second paragraph you wrote:

In vertebrates, Bmp is high in concentration along the ventral side of the embryo, opposite the developing nervous system.

Did you mean along the dorsal side? It looks that way in the figure.

And will this be on the test?

#36

Posted by: PZ Myers | May 7, 2007 10:37 PM

Good question. Bmp ventralizes vertebrate embryos. What's confusing is the topology: the dorsal most strip of the body wall sinks into the interior during neurulation, so the lowest concentration of Bmps is the neural tube, and it's roofed over with more lateral ectoderm that contains greater concentrations of Bmp.

Of course it's going to be on the test. Everything I say is going to be on the test.

#37

Posted by: Question | June 24, 2007 12:34 PM

Well, what I still don't get is from this story is the following. It was well known that the dorso-ventral distribution of markers was conserved in drosophila. The drosophila data are incorporated in the last figure of the post (and also in the paper). This organization is also conserved in other branches of the deuterostomia tree. So, then, yes, Platynereis is also a paralell branch of the Protostomia group, and no surprise it has the same distribution of markers than all the rest of the organisms analized. I do agree that the molecular characterization is extensive, but I don't see what it is so awfully novel in this story. What did I miss in the explanation? Can someone explain me the novelty of the strudy?

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