Thumbs down, what?

Bird fingers confuse me, but the explanations confuse me more, it seems.

I didn’t mean to post today, but I’ve just read a new review/hypothesis paper about the identities of the stunted little things that pass for fingers in the wings of modern birds. The review part is fine, but I’m not sure I get the difference between the hypothesis Čapek et al. (2013) are proposing and the hypothesis they are trying to replace/improve.

To recap: the basic problem with bird fingers is that fossil, genetic and developmental evidence seem to say different things about them.

1. Fossils: birds pretty clearly come from dinosaurs, and the early dinosaurs we have fossils of have five fingers on their hands with the last two being reduced. Somewhat closer to birds, you get four fingers with #4 vestigial. And the most bird-like theropods have only three fingers, which look most like digits 1, 2 and 3 of your ordinary archosaur. (Although Limusaurus messes with this scheme a bit.)

2. Embryology: in developing limb buds, digits start out as little condensations of tissue, which develop into bits of cartilage and then finger bones. Wing buds develop a short-lived condensation in front of the first digit that actually forms, and another one behind the last “surviving” digit. Taking this at face value, then, the fingers are equivalent to digits 2, 3 and 4.

3. Genetics: In five-fingered limbs, each digit has a characteristic identity in terms of the genes expressed during its formation. The first finger of birds is most like an ordinary thumb, both when you focus on individual genes like members of the HoxD cluster and when you take the entire transcriptome. However, the other two digits have ambiguous transcriptomic identities. That is, bird wings have digit 1 and two weirdos.

Add to this the fact that in other cases of digit loss, number one is normally the first to go and number four stubbornly sticks around to the end, and you can see the headache birds have caused.

So those are the basic facts. The “old” hypothesis that causes the first part of my confusion is called the frame shift hypothesis, which suggests that the ancestors of birds did indeed lose digit 1, as in the digit that came from condensation 1 – but the next three digits adopted the identities of 1-2-3 rather than 2-3-4. (This idea, IMO, can easily leave room for mixed identities – just make it a partial frame shift.)

Čapek et al.’s new one, which they call the thumbs down hypothesis, is supposedly different from this. This is how the paper states the difference:

The FSH postulates an evolutionary event in which a dissociation occurs between the developmental formation of repeated elements (digits) and their subsequent individualization.


According to the TDH no change of identity of a homeotic nature occurs, but only the phenotypic realization of the developmental process is altered due to redirected growth induced by altered tissue topology. Digit identity stays the same. Also the TDH assumes that the patterning of the limb bud, by which the digit primordia are laid down, and their developmental realization, are different developmental modules in the first place.

(Before this, they spent quite a lot of words explaining how the loss of the original thumb could trigger developmental changes that make digit 2 more thumb-like.)

I…. struggle to see the difference. If you’ve (1) moved a structure to a different position, (2) subjected it to the influence of different genes, (3) and turned its morphology into that of another structure, how exactly is that not a change in identity?

Maybe you could say that “an evolutionary event” dissociating digit formation and identity is different from formation and identity being kind of independent from the start, but I checked Wagner and Gauthier’s (1999) original frame shift paper, and I think what they propose is closer to the second idea than the first:

Building on Tabin’s (43) insight, we suggest causal independence between the morphogenetic processes that create successive condensations in the limb bud and the ensuing developmental individualization of those repeated elements as they become the functional fingers in the mature hand, thus permitting an opportunity for some degree of independent evolutionary change.

Am I missing something? I feel a little bit stupid now.



Čapek D et al. (2013) Thumbs down: a molecular-morphogenetic approach to avian digit homology. Journal of Experimental Zoology B, published online 29/10/2013, doi: 10.1002/jez.b.22545

Wagner GP and Gauthier JA (1999) 1,2,3 = 2,3,4: A solution to the problem of the homology of the digits in the avian hand. PNAS 96:5111-5116

12 thoughts on “Thumbs down, what?

  1. jdeangelis79 October 30, 2013 / 13:13

    I think that when the premise for research is false then the assembling of timelines and how it all works is just nonsense. Evolution is not a fact. Have a look at have a little read. No insult intended my friend

    • Naraoia October 30, 2013 / 13:54

      Harun Yahya is a kook who mistook a fishing lure for an actual insect. I think I’ll pass…

    • agnophilo November 1, 2013 / 18:18

      This guy also claims the holocaust was just some jews getting typhus and dying from famine… We have film reels of the death camps, which by the way, still exist in germany to this day, ovens and all.

  2. nick October 30, 2013 / 21:40

    their argument is further obstructed by relying on Limusaurus and conclusions drawn by Xu et al.

    i am also confused why they feel Eoraptor/Herrerasaurus being theropods or not matters as other baso-theropods and non theropod dinosaur/omorphs show the same pattern of asymmetrical digit reduction

  3. agnophilo November 1, 2013 / 18:14

    I recently read the book “your inner fish” which deals with the fossil, genetic and developmental evidence about the origins of our digits in fish, where they originated. Part of it talked about how if you introduce a form of vitamin A where two digits are growing you will get a mirror copy of them, and how other genes modify how they develop – in humans for instance one gene being broken makes us have paddle-like uniform fingers etc. So while the book didn’t exactly make me a geneticist there may be something in all of this which resolves your quandary. Maybe the mirror image digits were switched off but the “make this look like a pinky” genes were still active and modified the other digits, or something like that.

    I hope this loosely remembered information may be useful.

    Good book btw.

    • Naraoia November 5, 2013 / 11:55

      I’ve read Your Inner Fish too, it’s a really fun book.

      My problem isn’t with the biology, I think I have an OK grasp of that. I just can’t for the life of me tell the difference between two ideas these guys insist are different. 😀

      • agnophilo November 5, 2013 / 21:02

        It’s just confusion over which digit is which.

  4. Daniel December 16, 2013 / 12:00

    As the first author of the paper I have a few things to add to the discussion 😉
    First I appreciate your critique, since you obviously thought thoroughly about the problem.

    Now to the science:
    Again first:
    The main point of the paper is the mechanism that triggers the altered phenotypes of the digits: the concept that the loss of digit I itself causes the changes and the developmental processes behind them.

    Second: The identity and homology of the avian digits as well as of every structure with different positional and compositional criteria is a complex problem (we discuss those aspects in the final section of our paper, but also the Ramirez paper on this is pretty cool). The main objection was:
    “If you’ve (1) moved a structure to a different position, (2) subjected it to the influence of different genes, (3) and turned its morphology into that of another structure”
    Ad (1): you don’t move it to a different position; it still is at position 2, only that the digit from position 1 is lost in the adult. Saying it oversimplified: If somebody looses his thumb, it doesn’t make his index finger a thumb, just because it is the most anterior now.
    Ad (2+3): this is actually the point: if you subject a structure to a different chemical/physical or general developmental environment it is possible that it behaves differently.
    Ad (3): given the highly derived morphology of the avian digits (“the stunted little things that pass for fingers”), I think the morphology is not a strong argument. In the dinosaur ancestors this is a different story; I guess here the discussions are going on.

    So overall the difference between the TDH and previous models has to be seen on all 3 levels:

    On the homology level we argue that the digits receive/adopt an identity when they are formed and subsequently differentiate while they are growing. You would not call digit 2 “digit 1” as long as the digit 1 anlage is visible, so why would you later? It is true that the transcriptome looks more like the digit 1 transcriptome of the hind limb, but this is due to the mechanism we suggest in our paper.

    On the fossil level the frame shift hypothesis assumes that the digit reduction occurs on the posterior side, while the TDH – more like the pyramid reduction – allows for a bilateral reduction.

    On the developmental genetics level, we suggest a mechanism that alters the developmental outcome of digit differentiation, instead of assuming an evolutionary event in which the whole digit frame is shifted towards other embryonic positions. In this case our hypothesis explains the data (transcriptome, cyclopamine treatment, etc.), better then the frame shift hypothesis, although it is data from frame shift papers.

    I am fully aware and we explicitly state in the paper that we include elements from FSH and PRH in our model. This is because both have good points, but simply cannot explain all the data. In this way you can see the TDH as a compromise, based on the suggested morphogenetic mechanism.

    • Naraoia December 21, 2013 / 20:25

      Thanks for the clarifications! I think most of the misunderstanding is down to different concepts of “identity” 🙂

      I can’t remember exactly what parts of the paper I had in mind when I wrote the post, but just now I re-read the Morphogenetic and Biomechanical Aspects section, and this jumped out at me:

      soon as the development of the primordium for digit I ceases or
      merely lags behind the one of the other digits, cells that would
      usually contribute to the formation of digits II–IV, expand into a
      more anterior region where they partially behave as if they were
      digits I–III. The reason for this relocation is likely to be
      morphogenetic or biomechanical, rather than following from
      gene expression.

      To me, this sounded as though you were simply proposing a mechanism for a (partial) frame shift. Pre-digit 1 growth is reduced, that makes d2 spill over into d1 territory, encounter a d1-like molecular environment, and develop into a morphological d1. By my definition of “identity”, that totally is a change in identity. But in your comment, this happens:

      On the homology level we argue that the digits receive/adopt an identity when they are formed and subsequently differentiate while they are growing. You would not call digit 2 “digit 1” as long as the digit 1 anlage is visible, so why would you later?

      I see why I thought “WTF do you mean there’s no change in identity??” while reading the paper now. Yes, I totally would call that a d2–>d1 transformation, a bit like a T3–>T2 transformation in fruit flies. Just because that fly still has a proper T2 segment doesn’t mean it can’t have another one. 😀

      Posterior vs bilateral digit reduction: Ah, OK. Though Bever et al. 2011 tweaked the FSH to include the possibility of bilateral loss.

      (I hadn’t remembered that the FSH folks were so adamant about a sudden frame shift. [Bever et al., 2011] again: “the frame shift, by definition, must be a sudden, discrete event”. Huh? Aren’t they just making their own lives more difficult with that?)

  5. Daniel December 22, 2013 / 11:44

    Hi again,

    I’m glad I could make things clearer. We knew that the identity question will cause some discussion. the bird digits are not the only case where this problem exists, it is more a general problem of homology. It will be interesting to see where this will be going.

    I agree on your opinion of the Bever paper. They are making their lives more difficult, but what they say is stringent: if you argue that the whole frame is shifted then their is not much room for partial things. Xu introduced a partial frameshift model called the the lateral shift, based primarily on his Limusaurus. This is quite close to what we think happened in terms of fossil evidence. Currently the Limusaurus evidence is quite a debate among palaeontologists. Let’s see how that goes. It might have quite an impact on where digit 1 was lost (also for the frameshift people this will be important).

    • Naraoia January 15, 2014 / 17:14

      That sounds interesting indeed!

      As soon as I started reading it, I immediately thought of acanthodians. After a quick read, I see the paper doesn’t discuss them – so how do you think their numerous pairs of spines fit into this scheme?

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