Evo-devo of digital reduction in amphibians

ResearchBlogging.orgSynopsis: Alberch and Gale: “A Developmental Analysis of an Evolutionary Trend: Digital Reduction in Amphibians” (1985). In this paper, the authors looked at different foot morphologies in extant amphibians and performed some experimental embryology with a few of the species. The induced developmental change followed the natural variation found by the authors! Details below!

This post serves two purposes as:

1) My weekly devo post

2) Personal interest in the larger picture of evo-devo and how it relates to the Modern Synthesis. (Little surprise that I discovered this article through a Stoltzfus article!)

Alberch and Gale first examined the digital morphology, particularly the number of phalanges in hindlimbs, of extant amphibians. They excluded caecilians due to their limbless nature and focused on anurans (frogs) and caudates (salamanders). Interestingly, as of 1985, there was debate if frogs and salamanders are mono- or polyphyletic (meaning did the two groups arise from different ancestors)? This is due to different developmental pathways, one which we will explore here (although that is not the ultimate point).

Alberch and Gale focused on digital reduction and they noticed patterns within each taxa. This makes sense as frog digit development starts from the middle and proceeds outward while Salamander digit development is sequential – from I (“thumb”) to V (“pinky”). The pattern Alberch and Gale noticed was that frogs initially lose I and V (the outer digits), whereas salamanders lose V/IV (the last digits). This is shown in frogs in Fig 1.

The authors further decided to mess around with the developmental process by adding colchicine, a mitotic inhibitor, to the developing limb bud, subsequently reducing the number of cells found within. The patterns of the “mutated” (these aren’t genetic changes) limb buds followed the natural morphological patterns!

Fig 2: a) Dorsal view of the left foot of salamander Hemidactylium scutatum (a 4-toed lungless salamander). b-c) The two feet of a fully developed axolotl Ambystoma mexicanum. The right foot (c) is the untreated control, while the left foot (b) has been treated with colchicine at the limb bud stage. Notice the left foot (b) is smaller than the right foot (c), and also notice that the morphology of (b) closely resembles (a), a foot of a different species, in digit number and phalanges number per digit. Also note the differences in the tarsals.

Figure 2 is particularly evocative. By messing with the left limb bud of (b) (same species as c)), the resulting foot resembles that of a), a different species. Specifically, the phalanges number per digit is the same between a) and b):

The phalanges formula (from I to V) (take heed of the mirror images of Fig 2):

a) 1-2-3-2-0
b) 1-2-3-2-0
c) 2-2-3-4-2

That is a major difference. Also notice that b) is physically smaller than c), which is not surprising considering colchicine reduces the number of cells available to the developing limb bud.

Is this a case of “simple developmental truncations”? In other words, are these differences a result of development just stopping at a certain point? This is possible considering the salamander is losing digit V (remember sequential development), but Alberch and Gale argue no. Here is why.

Fig. 3: Sequence of metatarsal and phalangeal differentiation in the salamander, A. mexicanum (the changed species from Fig. 2). Stippling indicates early stages of chondrogenesis (cartilage formation).

Look at normal left foot development (Fig 3) in Ambystoma mexicanum (the axolotl changed in Fig 2). If development were to stop before the formation of digit V (the leftmost digit in this figure), the foot would be somewhere between the 4th and 5th depicted stages. The resulting phalanges formula would be 2-2-3-1-0. However, as we saw in Fig. 2, the resulting foot due to the “mutation” is 1-2-3-2-0. Clearly the two do not match. This is depicted in a different species in Figure 4c and 4d. (Fig. 4a and 4b depict the change of Fig. 2).

So “simple development truncation” does not support the results. Instead, Alberch and Gale state that mutations would have to affect the limb bud in similar ways to the mitotic inhibitor, colchicine. Examples include dwarfism (reduce the absolute number of cells) or a “slowdown in the rate of cell proliferation associated with paedomorphosis. Dwarfism may be likely as evidenced by Fig. 2 and by more data collected by Alberch and Gale.

Alberch and Gale (and subsequently, Stoltzfus) argue for a larger idea which I will discuss in my next weekly devo post (this one is long already!). Alberch and Gale argue we must revise how we think of developmental constraints. In turn, Stoltzfus argues that the Modern Synthesis cannot take these developmental biases into account and that we must come up with a new synthetic theory of evolution. Find out why next week!
Alberch, P., & Gale, E. (1985). A Developmental Analysis of an Evolutionary Trend: Digital Reduction in Amphibians Evolution, 39 (1) DOI: 10.2307/2408513

19 thoughts on “Evo-devo of digital reduction in amphibians

  1. Didn’t read the paper, but I might have to now ;) You wrote…

    In turn, Stoltzfus argues that the Modern Synthesis cannot take these developmental biases into account and that we must come up with a new synthetic theory of evolution.

    A few questions…
    Quick definition of “Modern Synthesis” so we know what we’re working with?
    How does that definition of the Modern Synthesis fail to “take these developmental biases into account”?
    What revision(s) to the Modern Synthesis would fix that inconsistency?


    • Good questions!

      I will try to answer those questions in next week’s posts. Thank you for addressing what the “Modern Synthesis” even is – I’ll be sure to write up a working definition of that as well, seeing as I mention it so frequently.

      I don’t think you’ll find your answers in the Alberch and Gale paper. If you want to “read ahead,” however, you can check out the Stoltzfus paper I mention.

      Stoltzfus A. “Mutationism and the dual causation of evolutionary change.” Evolution & Development. 2006;8(3):304-17. ] http://www.ncbi.nlm.nih.gov/pubmed/16686641.


  2. Ok. I want you to succeed. So I’m going to be critical and hold you standards that, maybe you think are not “fair.” But I’m not interested in “fair,” but, as I said, in your success.

    1. Punctuation and grammar are important. Even for scientists. My wife is a scientist and she has me review each and every paper she writes and makes virtually every editorial change I suggest for the sake of clarity. I’ll forgo marking-up your post. But, please, write, read, edit. Then, set it aside for a few hours and go back and repeat the process. It will help tremendously.

    2. This paper is old. Did you use the citation in any search function to see how much impact it may have had? Any criticisms of the paper? Any follow-up research that would reinforce or contradict this research?

    When I plugged in the citation, I noticed a number of papers that referred to this paper. However, since they were all behind pay-walls, and I refuse to use my wife’s university account to get them for free, I can’t speak to the verification or refutation of the ideas in the paper you reviewed.

    3. Less colloquialism. We’re not a couple of ‘dudes’ talking about a football game, instead you’re describing something technical to an audience. And while I don’t expect you to write like there is a stick in your bum… Remember to whom you are writing, and it’s probably not the guys on your WoW raid, or were at last night’s kegger party (do they still call them that?)…

    4. Why would we need to “rethink” modern synthesis? Further, as a warning, always be concerned when someone is trying to over-throw/redefine an accepted scientific paradigm. Modern Synthesis is older than Dr. Myers, myself or you and, while it’s made some adjustments, it has proved to be quite robust.

    5. You seem really excited about your subject. It comes through. Don’t lose it. But learn to modulate it, it will help your writing remain focused.

    6. When using a technical term (caecilian in this case) tell your audience what it means. Do not assume everyone knows they are legless amphibians that resemble snakes and/or worms. I only know by pure, stone-cold luck. I’m not sure my wife, a developmental biologist at Washington University Medical School would remember. And she’s a PhD research scientist.


    • Thought I’d share two cents on MosesZD’s comments.

      1. I totally agree with. Punctuation and grammar are important and this really is a good habit to pick up:

      …write, read, edit. Then, set it aside for a few hours and go back and repeat the process.

      2. Follow-up is important, but can be time consuming and costly w/o journal access. Always give it some consideration, and maybe direct readers to do their own follow-up if you feel there might be an interest. If UMM has access to ISI web of knowledge, learn to use it.

      3. I’d say “careful with colloquialisms”. Depends a lot on your target audience, the subject of the post, etc. The gold standard here is whether or not you’re communicating effectively with a broad audience. Jargon can be just as bad as colloquialisms, and just as useful.

      4. Clear motivation is always good, right up front and crystal clear.

      5. Err on the side of excited. Like good food, a bit tad too much flavor is better than something a little bland.

      6. It looks like you already do this, but remember that this isn’t paper. I prefer to hyperlink technical terms or jargon to point readers to key details. Putting some text as the “title” in the link shows on mouse over in some browsers. Ideal for something like caecilians. This also works with some of the more colorful colloquialisms ;)

      Finally, if you’re lucky enough know any good writers, English majors, etc. hound them to critique your posts. Fortunately, blogs allow you to easily go back and make minor edits as needed ;)


    • Moses,

      Ok. I want your comments to succeed. I really do. But your feedback had some glaring weaknesses that I just can’t accept. To wit:

      “So I’m going to be critical and hold you standards that, maybe you think are not ‘fair.'”

      There should be a “to” in between “you” and “standards,” no? Something tells me this isn’t the first time you’ve used this exact same phrasing, either, so why, after the second or third cut-and-paste job, didn’t you realize your error? There also isn’t a need for a comma after “that.”

      Too pedantic? I’m sorry, but like I said, I’m only interested in your success, and I don’t want a perfectly good commenter to be disregarded merely because he decided to carelessly elide certain words or ignore punctuation rules. I’d also be remiss if I didn’t point out that, in your following sentence, you used the word “but” twice; ease up there a little, dude. (Sorry, too colloquial?)

      Seriously, though, don’t repeat words like that. It’s a simple case of avoidable redundancy, and it makes it seem like you didn’t re-read your work for redundancy. See how annoying that is?

      A few other things to note:

      – Use elipses with more care. Calling on them twice in quick succession (see: your third point) makes it seem as if you’re unfocused and whimsically drifting in and out of thoughts.

      – I’ve never seen the word “overthrow” hyphenated.

      – Saying things like, “Remember to whom you are writing” creates some seriously convoluted syntax. Latin prohibits ending sentences with prepositions, but English has no such rule (and besides, that was only a clause). “Remember your audience” would avoid the problem entirely. Always think “reword” before “rearrange.”

      I hope you don’t think I’m being unfair with my critique. Like I said, I’m only interested in your success. I still think – provided you keep practicing your craft while taking my advice seriously – by the end of the semester you’ll be a crackerjack (too colloquial again?) blog commenter.


  3. I have to disagree with MosesZM. I work in editorial (including a trade science imprint) and I consider the writing style ideal for a blog. This is not a formal piece destined for a science journal, after all. And frankly, the grammar and punctuation are better than what I see from the majority of our published authors.

    That being said, I’m off to check out the feet on my pet azolotl.


    • I have to agree with Erika on the tone of your post. I will agree with ZD in that I’d would have liked to have seen some more about more recent research in this area. This was an area of interest to me looonnngggg ago when I was an undergrad, so keep it up.


  4. I’m impressed with the post. Blogging is essentially story telling, and you are doing exactly that. Other commenters have noted the fact that the paper is old. What this really means is that it would be good if you could articulate why you have picked this paper to write about, since it isn’t shiny and new.


  5. I’ll try to respond to the general ideas behind the comments.

    Yes – grammar, punctuation, tone, etc. are all important. Telling me that is not entirely helpful though. Are there examples of where I totally goofed?

    I spent about 3 hours reading the article and writing it up and by that time I just wanted to throw the article out here. I did reread everything I wrote at least once though and made some major edits in the process. However, as ErikaM said, this is a blog, not a professional journal. While I intend to keep my writing to a fairly high quality, I’m not writing a paper that is 20% of my grade. I don’t know if anyone who has commented has experience writing up posts like this or not, but it’s pretty damn hard and time-consuming, especially when you’re not an expert. I’m not trying to complain here – I’m just telling you not to expect an A+ paper.

    Normally I do at least link to Wikipedia articles for jargon (as in paedomorphosis in this one), but overlooked it for the most part. I’ll be sure to keep that in mind in later posts.

    Moses, I’m honestly confused by what you are saying about my tone. How am I being colloquial and talking to a couple of ‘dudes’? I try to keep a fairly serious tone here and I believe I did just that.

    As for the content itself,

    Yes, this is an old paper but I had never heard about it before. As I say in the beginning of the post, I stumbled across this in Arlin Stoltzfus’ 2006 article (linked in an above comment) and decided to read the paper itself to better understand Stoltzfus’ point. As I’m now just jumping into the literature, I have little perspective on how the article relates to the history of evo-devo. This will hopefully fix itself with time.

    Also, in PZ’s class we have to write a 5-10 page paper on any devo topic we choose. I have decided to write on developmental constraints so expect to read more about this topic as the semester progresses.

    As for rethinking the Synthesis – I have an inherent distrust of orthodoxy. Evolution is far from settled and I doubt all there was to know about how evolution works was known in the mid-20th century. Yes, we should be careful about what revisions scientists advocate, but we should also be careful not to just trust what people thought 60 years ago.

    Thank you for the comments everyone! Now is there anything wrong in my post content-wise? :)


    • lolz.

      No. You don’t format an email like a formal letter; you don’t format a blog post like a journal article. I think of a blog as being more like a discussion. This is an awesome post, keep it up :)


    • I thought that this post and your blog in general was incredibly interesting, and I too enjoy your tone and subject matter. Please keep up the good work.

      About grammar: I’m not going to go through your post and nitpick, particularly because I didn’t see any major errors. I’ve found that the best way to have good grammar and spelling automatically, the first time you type something, is to be careful about those things in everything you type, no matter how trivial. It does take a long time, but after a while it should get easier.

      I’m looking forward to next week’s post!


  6. Paul –

    I looked for an option to enable comment previews but couldn’t find one. I know they are available on wordpress.org, but wordpress.com can be severely limited when it comes to features (however basic). Googling the issue didn’t seem to help either – users request it and WordPress doesn’t answer.


  7. At the risk of being wrong, I think Moses might have considered the phrase “mess around” too colloquial. If it were a journal article, I would agree, but not on a blog post. It’s up to you to decide whether you consider the blog to be practice for writing papers, or whether you are developing your blogging style. To me, it had the tone of a paper, except for the odd phrase (like “mess around”).

    As for punctuation and grammar, the only thing I would watch is your use of parentheses. In my own writing, I tend to use parentheses when I haven’t got the words flowing yet. So in this post, “anurans (frogs)” is fine, but “The phalanges formula (from I to V) (take heed of the mirror images of Fig 2)” is a little awkward.

    One thing I will say is that you are being held to a high standard because you clearly have ability. I recognise the amount of work that went into this blog (I think we all do). Don’t consider it a waste of time, because this effort will pay off big-time as you are integrating the material you are studying, retrieving it, and presenting it all at the same time. We are not born writing well; it’s a long process getting it right. You are well on your way.


    • Okay, those make sense. Indeed, parenthetical statements and language such as that imply uncertainty and ambiguity. I will make an effort to avoid those in the future. Thank you for finding examples!


  8. I think you should not be concerned about linking every word that might be unknown to those of us not in the field. It’s a blog! We who are reading it are on the internet, and it’s a simple thing to pop open another tab to google a term. I do it regularly when reading science blogs.


  9. Nice classic paper, Kele.

    Firstly, it’s clear to me that you have a pretty good understanding of the paper and its context in the literature, which is cool.

    As for your writing style:
    I think you could work on your writing to make it easier for your audience to read. It’s OK at the moment, but with some good editing for readability and flow it could be much better. Writing clear, elegant prose is something all scientists need to work on. I’m not saying it needs to be formal in tone or anything, it just needs some tweaking here and there.

    For example: “By messing with the left limb bud of (b) (same species as c)), the resulting foot resembles that of a), a different species. ”
    This sentence winds itself in knots, and I had to re-read it. Ultimately you want to always avoid having your reader have to re-read things or skip to and from different passages.

    Another example: “Alberch and Gale focused on digital reduction and they noticed patterns within each taxa. This makes sense as frog digit development starts from the middle and proceeds outward while Salamander digit development is sequential”
    As soon as you said “This makes sense as….” I started to feel like I was missing something, because you hadn’t yet explained what those patterns were.

    I would have liked you to rearrange that paragraph to say something along the lines of, “…they found patterns within each taxa, with frogs tending to lose digits I and V (the outer digits), and salamanders tending to lose digits IV and V (the most posterior digits). Frogs’ and salamanders’ digital development differs in the order of digits developed first [explanation], so these observations make sense if what has happened over evolution is the loss of digits that develop latest. Alberch and Gale wanted to test this hypothesis… etc etc”

    Now onto the content:

    Tell me (your reader) what Modern Synthesis is! Some people may need reminding, and want to know how this paper fits into that context. Although you’ve discussed it on your blog before, each post should be able to be read and understood without too much reference to past posts.

    Why do A. and G. argue that we need to revise our ideas about developmental constraints? This is an interesting area and I would have liked to see just a wee bit more explanation here.

    I see that you’re planning to continue your discussion on this paper later on, but I reeeally wanted that discussion to occur in this post. What was it about this paper that lead to the authors arguing for a rethink on modern synthesis? What do we think about this paper now, in the context of current knowledge of limb development?

    Anyway, good job, keep up the good work, and I hope my critique is useful to you in some way!


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