Friday, March 30, 2007

Animal Chauvinism

 
There's much to criticize in the field of evolutionary developmental biology or evo-devo. Some of the "theories" are little more than wide-eyed speculation. I'm thinking particularly of The Plausibility of Life by Marc Kirschner and John Gehart.

The thing that bugs me more than anything else is the attempt to create a general theory of evolution based entirely on a subset of living species; namely multicellular animals. Most proponents of evo-devo seem to be entirely unaware of the the fact that there are other species where genes are developmentally regulated.

This strange bias is spectacularly illustrated in a recent review in Nature Reviews: Genetics. The authors, Ronald Jenner and Matthew Wills, say,
Study of the model organisms of developmental biology was crucial in establishing evo–devo as a new discipline. However, it has been claimed that this limited sample of organisms paints a biased picture of the role of development in evolution. Consequently, judicious choice of new model organisms is necessary to provide a more balanced picture. The challenge is to determine the best criteria for choosing new model organisms, given limited resources.
Great! I couldn't agree more. When I used to teach this stuff I would begin with development in bacteriophage lambda where there is a beautiful example of a genetic switch. I then described development during sporulation in the bacterium Bacillus subtilis where there's a nice simple example of communication between the mother cell and the developing spore. Both of these examples made it into my textbook back in 1993.

Yeast development got a lot of play in my courses and it still does in the courses that are taught here. I would also look for examples of plant development since that's where I first learned about development as an undergraduate. We need to teach more plant development.

So, as you can imagine, I was excited to read the abstract of this paper. Jenner and Wills bemoan the fact that most of the work in the field is based on just six model organisms: Caenorhabditis elegans, Gallus gallus, Xenopus laevis, Mus musculis, Danio rerio, and Drosophila melanogaster. How right they are. The evo-devo crowd needs to expand their horizons to cover bacteria, protists, fungi, and plants.

So I eagerly read on to see which organisms they would name. Here are their choices: sea urchin, dung beetle, water flea (Daphnia), and sea anemone. All animals.

Evo-devo is never going to gain widespread respectability among evolutionary biologists unless the proponents abandon their animal chauvinism and start to recognize that development is important in four other kingdoms. [Press Release from the University of Bath]
Jenner, R.A., Wills, M.A. (2007) The choice of model organisms in evo-devo. Nat Rev Genet. 8:311-314. Epub 2007 Mar 6.

23 comments :

  1. There is plenty of plant evo-devo going on, though within that area it might be fair to complain of bias in favor of the evolutionary origins of flowering plants(but a little literature searching ought to convince you that that, at least, is quite an active field). It's probably also fair to complain that the animal and plant people might not be as aware of one another as they ought to be, though the basic principles and machinery of multicellular existence are rather different as between animals and plants.

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  2. Damn, why is that redirection failing? Anyway, it was just a Google search on the keywords plant evo devo. Try it.

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  3. You scooped Pharyngula. Even though the embellished press release I saw had a zebra fish embryo illustration...

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  4. How does the Hardy Weinberg principle relate to the meta analysis of the 4000 species of mammals published on Nature?

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  5. four other kingdoms

    What would those other 4 kingdoms be? Plants, animals, archaebacteria, eubacteria, and protists? If you say the protists are a "kingdom", I'll be totally bummed. Let's abondon that 5 kingdom system ASAP.

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  6. Small slip: you've got Drosophila melanogaster listed twice in the list of six.

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  7. @rpm: the usual list of 5 is prokaryotes, protoctists, fungi, animals and plants. What better set would you like to propose?

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  8. rmp asks,

    What would those other 4 kingdoms be? Plants, animals, archaebacteria, eubacteria, and protists? If you say the protists are a "kingdom", I'll be totally bummed. Let's abondon that 5 kingdom system ASAP.

    Yes, I'm saying protists are a "kingdom." You can't ignore them even if they're polyphyletic.

    Please let me know what your favorite classification is and how you propose to deal with protists. I've never heard of a satisfactory alternative. Do you have one?

    BTW, the fifth kingdom isn't archaebacteria. It's fungi. But you knew that, didn't you? :-)

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  9. Steve LaBonne says,

    There is plenty of plant evo-devo going on, ...

    I know that. That wasn't the point. The point is that the leading proponents of "evo-devo" as a new way of looking at evolution tend to focus almost exclusively on animals.

    There's lot of talk about HOX genes and compartments (or segments) and determination. They don't seem to understand that other species can do it differently.

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  10. Pretty offtopic, but I thought you might appreciate this:

    http://tinyurl.com/2ume8o

    Redirects to a thread on the SomethingAwful forums. If you're not familiar with it, it's a large (90k+ users), heavily moderated (one time registration fee) forum.

    The interesting thread: "Ask me about being Dr. Michael Behe's daughter"

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  11. The point is that the leading proponents of "evo-devo" as a new way of looking at evolution tend to focus almost exclusively on animals.
    There's no doubt the plant people need to advertise better- that might help with the age-old disparity in funding, as well. It would be great if someone working on plant evolution could produce a popular book as appealing as Sean Carroll's.

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  12. Please let me know what your favorite classification is and how you propose to deal with protists. I've never heard of a satisfactory alternative. Do you have one?

    You can treat the eukaryotes properly. Protist, to me, is synonymous with eukaryote because it captures the majority of the eukaryotic diversity. I like this breakdown.

    Plants remain, but they include land plants, green algae, and red algae (ie, eukaryotic autotrophs). Animals, along with fungi and some of the "protists"), are unikonts. The rest of the "protists" fall into three other groups.

    I'll leave organizing prokaryotes to someone else.

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  13. rpm says,

    You can treat the eukaryotes properly. Protist, to me, is synonymous with eukaryote because it captures the majority of the eukaryotic diversity. I like this breakdown.

    The proposed scheme would be wonderful if it were true. The problem is we don't have a very good idea about protist phylogeny. Until we do, we have little choice but to stick with the old five kingdoms.

    Some people think we will eventually construct a reliable tree like the one shown in your reference. I'm not very optimistic. I don't think the quality of the data is good enough to resolve the deep nodes in the eukaryotic tree. The one thing we know for sure is that the ribosomal RNA tree is wrong.

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  14. "The proposed scheme would be wonderful if it were true."

    It is a damn sight truer than the old five-kingdom system. It is also where (or very close to where) the current consensus lies amongst experts in the field. Check out as well Adl et al.'s 2005 paper in the Journal of Eukaryotic Microbiology, 52:399-451.

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  15. Somebody said,

    It is a damn sight truer than the old five-kingdom system.

    In one sense it's truer but in another sense it isn't. The good sense is that your suggestion is much more rationale and more representative of real eukaryotic phylogeny. The bad sense is that we don't know if it's correct.

    At least with the Five Kingdoms we know that three of them (fungi, plants, animals) are true clades. Probably bacteria are as well.

    The problem with most proposed revisions is that we run a very high risk of making all the new kingdoms polyphyletic (or worse) within a few months of accepting them.

    We're not ready for new kingdoms yet. That's why we're stuck with the old system for now.

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  16. "The bad sense is that we don't know if it's correct."

    Certainly some of the details are still disputable. But I see nothing wrong with recognising that, for instance, alveolates and stramenopiles are kingdom-scale clades, and calling them kingdoms. Whether or not the Chromalveolate Hypothesis is correct, the lineages that make it up are pretty well supported. Even if we do mailtain some grab-bag taxon (such as Protista) for those organisms of debatable affinity (say, the excavates), there is no reason to shoehown the eukaryotic diversity about which we have no uncertanties into the same grab-bag.

    Personally, I have no problem with recognising twenty or thirty eukaryotic kingdoms, and leaving the details of their interrelationships to ongoing investigations. The same thing happened with animal phyla a hundred-plus years ago, after all.

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  17. How nice to see The Plausibility of Life by Marc Kirschner and John Gerhart called wide-eyed speculation. I found this book ignorant of anything beyond vertebrates (even if they do know a lot about vertebrate development), ignorant about evolutionary biology and especially ignorant about the topic they said they wanted to write about, the origin of novelty. After all, The Plausility of Life contains no account of the origin of any novelty whatsoever.

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  18. Heleen, I couldn't agree more.

    Some of the commenters are missing the point about evo-devo. The evo-devo movement is very animal centric. This is not to deny that that there's lots of developmental biology going on in botany and microbiology.

    The point is that the most vocal proponents of "evo-devo" are those who are making grandiose claims based almost entirely on studies of complex animals.

    The criticism of Kirschner and Gerhart applies to Sean B. Carroll. In his book Endless Forms Most Beautiful: The New Science of Evo Devo, he present an animal view of development. Some of the statements in that book are outrageous. I was especially shocked by this sentence in the preface.

    Not a single biologist, for example, ever anticipated that the same genes that control the making of an insect's body and organs also conrol the making of our bodies.

    Really? When I was growing up we fully expected that the regulatory genes discovered in bacteria and 'phage would have counterparts in eukaryotes. When HOX genes were first sequenced they were thought to be related to bacterial genes like lac and cro repressors. Nobody was surprised at that.

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  19. If microbiologists have always assummed that any molecular mechanism they uncover in any organism in principle must be applicable to all other organisms, it does not mean they have been illuminated from above, it means that they are wrong. Differences can evolve, from bacteria to bacteria, bacteria to animal, etc
    Comparisons of animals to bacteria can only be made at the level of the single cell. Now if you say "genes of dna replication", both bacteria and humans replicate DNA. It's not so surprising that many genes of basic molecular mechanisms described in bacteria will be the same as in humans. Eukaryote genes must have "bacterial" precursors. Even so, the similarities stop quickly. "Bacteria" can have substantiallly different metabolisms,environments, and energy sources that would suggest important genetic differences with animals.
    In animal patterning, it was not so obvious there would be any great molecular similarity. Many things were thought to be adaptive convergence, with no particularly similar molecular mechanisms of patterning.That turned out to be wrong.
    I just want to add that precisely BECAUSE discoveries in one gropu may not be applicable in another, is it that we must increase taxonomic sampling. And the reuts are not always as some would a posteriori describe as "the obvious"

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  20. Alipio said,

    If microbiologists have always assummed that any molecular mechanism they uncover in any organism in principle must be applicable to all other organisms, it does not mean they have been illuminated from above, it means that they are wrong.

    Really?

    First, let's make it clear that it wasn't "microbiologists" who made that assumption. It was almost everybody who was working at the molecular level. That includes biochemists, molecular biologists, and developmental biologists.

    Back in 1967 when Jacques Monod said, "What's true of E. coli is true of the elephant" he wasn't being ornery. He was expressing a common belief. It was a belief that the underlying biochemistry and molecular biology of all species were similar.

    Second, don't get confused about the difference between phenotype and its underlying cause. At the molecular level we're dealing with the regulation of gene expression. That involves proteins that bind to DNA. It's the same principle whether the effect is expression of the lac operon or the development of very long noses.

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  21. I thought François Jacob had said that.
    So proteins that bind dna that affect gene expression are present in bacteria... why would you expect something like that NOT to be present in animal cells? As I said, that is easily expected, because it is a very basic function, at the level of the workings inside a single cell. But what about the role of genes in DEVELOPMENT, of a multicellular organisms? It's evo-DEVO, after all. And here, I insist, it was not that easy to know that the same genes were involved in dorso ventral axis patterning, or eye development, etc. Not quite as easy as foretelling "dna-binding proteins will regulate gene expression", right?

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  22. Don't make me list the kind of things going on with eukaryote dna that do not go in bacteria...
    or, at the developmentla level, the accumulation of developmental patterning genes that have turned out NOT to be the same in different groups of animals.
    Sure, there are lots of similarities, but differences do exist, that is why we need to see more different kinds of organisms, ok? If not only a few (bacteria?) would suffice for all

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