Sunday, October 26, 2008

The Spandrels of San Marco and the Anomalocaris Paradigm

The Spandrels of San Marco and the Panglossian Paradigm is one of my favourite science papers. As someone who accepts natural selection as a powerful evolutionary mechanism, but who considers that there are other, equally, or perhaps more, powerful mechanism out there, such as genetic drift, this paper resonated a lot with me. To summarise the paper (if you haven’t read it, please do), not everything that happens in evolution occurs because it was selected for. Like spandrels, things can happen as a consequence of other events. To summarise the summary, sh*t happens.

Here I’d like to develop that theme using Anomalocarus.

Anomalocaris was a torpedo-shaped, 1+ metre, top-line predator in the Early Cambrian oceans. It had a nasty set of jaws set in a circular mouth and a pair of muscular spiny appendages
hanging praying mantis-like from the head, and a pair of large bulbous eyes. It was a mean bugger. If the kids that burn the wings off insects had aquaria, this is what they’d want in it. We’re talking the king of the Cambrian. Nasty.


Big predators need big prey and Anomalocaris ate trilobites, big trilobites, big spiny trilobites. In this case, Redlichia. (see image. Scale bar at top = 1cm)

Think of Redlichia as having the style, sophistication, and armour plating, of an Abrams tank. Not the quickest trilobite around, not the most manoeuvrable, but not so much of a problem when, you’re up to 20 centimetres long, and the only thing that big enough to eat you is Anomalocaris, especially when the jaw elements of Anomalocaris were less strongly mineralised than Redlichia, AND, the jaw elements couldn’t actually bite together!

Hang on. If the jaws were less strongly mineralised, and didn’t even come together strongly, just how could Anomalocaris eat Redlichia?

Well we have evidence that Anomalocaris did indeed eat Redlichia – trilobite fossils with great wedge-shaped bite marks that had to have been made by Anomalocaris, and fossil poo of broken Redlichia fragments of a size that could only have been delivered by Anomalocaris (at least we haven’t found anything smaller with an appropriately pained expression). Anomalocaris was able to dine on Redlichia by exploiting a weakness in one of the most successful body parts ever to have evolved, the arthropod exoskeleton.

OK, a quick intro to arthropod exoskeleton

Arthropod exoskeleton gets its mechanical properties primarily from a bilayered construction, consisting primarily of a thin, usually mineralised, outer exocuticle, underlain by a thicker, unmineralised, endocuticle. Each of these brings a differing mechanical property to the exoskeleton. The hardened exocuticle is strong (and thus resistive to cracking) under compression (or being poked), but weak (and vulnerable to cracking) under tensional forces (or being stretched). By comparison, the softer, more pliant endocuticle is the opposite, weak under compression, but strong under tension. These properties combine to provide a greater level of protection against mechanical attack than either layer could alone, especially against normal predation, which pushes down, producing compressional stress on the exocutile, and causing the underlying endocuticle to stretch around the pressure, producing tensional stress on the endocuticle.

By varying the thickness and mineralization of the two layers, arthropods can produce a wide range of exoskeleton types, from stretchy elastic to hard rigid.

(There’s a lot more to arthropod cuticle, but that’s enough to be going on with.)

Ok, so how does this help Anomalocaris, and where is the weakness? Well, what Anomalocaris did was to attack from the side, reach over the top of the trilobite with its two appendages and grip the far edge of the trilobite, wedging it between the spines on the appendages. It then pushed the near side of the trilobite into its mouth and pinned the trilobite in its jaws somewhere between the near side and the middle of the body. Now comes the neat bit. Anomalocaris would then pull up with its frontal appendages (no doubt assisted by the large muscles in the head) and flex the trilobite - almost like trying to roll the far side of the trilobite around to the near side to make a tube. Then Anomalocaris would reverse the process. Flexing one way imparts compression stress on the exocuticle and tensional stress on the endocuticle and flexing the other way reverses the stresses so that the exocuticle is under tensional pressure and the endocuticle is under compression. And as strong as both are in one stress field, they are weak in the other field. Flexing back and forth quickly induces fractures in the cuticle, which propagate and finally result in failure, allowing the Anomalocaris to break off large chunks of juicy trilobite.

You can mimic this process using a credit card (preferably an expired one). It’s impossible to break a credit card by poking at it with your fingers. But, if you grip it in both hands by the short edges and flex it back and forth, a line of weakness quickly forms, as plastic is weak in tension and the stretching motion quickly weakens the card. Pretty soon you can break the card as a crack propagates along the line of folding. Substitute appendages and mouth for your right and left hands and this is essentially what Anomalocaris does.

All well and good, but what has all this to do with evolution and spandrels?

Well, the thing about trilobites is that, as arthropods, especially arthropods with armour plating, the only way they can grow is by moulting.

Just as crabs do today, trilobites had to escape from the exoskeleton they were living in order to grow. They would emerge soft and squidgy, pump themselves up to the new size and then harden the new exoskeleton.

Prior to moulting, arthropods made changes to the cuticle that made it brittle and easy to crack. To further help the moulting process in trilobites, there were a series on lines of weakness, called suture lines. These were the first things to break once moulting started, and so aided the process. They can be seen in the Estangia photo at the top left of this blog. The crescent-shaped structures on the head, either side of the central bulbous glabella, are the eyes. The line running behind the eye and continuing on to the back of the head, is a facial suture. It continues from the top of the eye to the outer margin of the head – best seen on the left side of Estangia, where the whole area of the head outside of the suture line has been displaced (called the ‘free cheek’ for this reason). This shows that the specimen is a moult. Once the suture lines had parted, the trilobite would exit the old exoskeleton through the head region.

The reasons for suture lines around the eyes are obvious. It was important to ensure that the eyes were easily released during moulting, as the trilobite was vulnerable, and needed the eyes free to keep watch.

However, moulting is a hit and miss affair. Problems can occur. For example the facial sutures may not break easily. Trilobites having difficulty moulting would be in trouble, after all, it’s not like they could ask for help! A trilobite thrashing around on the sea bed trying to moult would draw attention to itself at a very vunerable time.

The problem for big Early Cambrian trilobites like Redlichia is that they had limited flexibility (curling head to toe). This meant limited options should anything go wrong with the moulting process. And things went wrong - I collected a Redlichia specimen where the left free cheek was upside down, the right was implanted into the sediment at 90 degrees, and the body has split into three parts. It had either undergone a horrendous moult, or had just had the best sex of its life!

So anything that assisted the moulding process would be advantageous

The ability to enrol the body (curling the body so that the head tries and meet the tail, with the legs tucked in between), even part way, would clearly aid moulting as it would stretch, and put pressure on, the exoskeleton and suture lines. So its of no surprise that by the end of the Cambrian all trilobites could flex to a fair degree, and some could almost touch head to tail. Estangia was well on the way to being able to do it in the Early Cambrian.

Enrolling has such an obvious benefit to trilobites generally that it isn’t surprising that it is a common, in fact pretty much ubiquitous, feature of trilobite after the Cambrian (the group that Redlichia belonged to never made it out of the Cambrian). Even the itty-bitty trilobites that Anomalocaris wouldn’t be seen dead eating (or rather would be seen dead as small trilobites wouldn’t provide enough energy to warrant the chase. Imagine a whale eating krill, one at a time!) It’s clear then that enrollment was probably selected for as an aid to moulting as pretty much all trilobites after the Cambrian could do it to a significant degree.

But, and here’s the kicker (finally), enrollment – even partial enrollment achieved by some Cambrian trilobites – negates the Anomalocarus predation method.

A curved trilobite cannot be flexed back and forth like a relatively flat trilobite can. To go back to the credit card analogy, imagine trying to flex a curved credit card.

Clearly enrolling didn’t evolve as a defence mechanism because the early, non-complete enrollement forms still allowed access to the softer juicier bits, and also would not have protected against adverse environments either. Neither could its common occurrence be put down to protection against Anomalocaris predation, as it occurs across the range of trilobites, even the itty-bitty ones.

The most obvious reason for enrollment in most, if not all, trilobites after the Cambrian, is that it aided in moulting and not defence, and not defence against Anomalocaris.

But it was the death-knell for Anomalocaris.

Anomalocaris was crucified on the spandrels of San Marco.

Sh*t happens.

Gould, S. J. and Lewontin, R. C., (1979) The Spandrels of San Marco and the Panglossian Paradigm: A Critique Of The Adaptationist Programme. Proceedings Of The Royal Society of London, Series B, Vol. 205, No. 1161, pp. 581-598.

21 comments:

  1. Wow. What a fantastic post!

    Hi, I'm Kate *waves*. I found your blog via John (Evolvingthoughts) (My blog is http://mnemosynosis.livejournal.com)

    I've created a livejournal rss feed for your blog -> http://syndicated.livejournal.com/ediacaranblog/profile so that your posts come up on my news feed.

    I look forward to many more!

    Cheers,
    Kate

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  2. Might not little baby Anomalocarises like to eat itty-bitty trilobites? A big Anomalocaris must have started life as a little 'un!

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  3. Yo, Chris -- Welcome to the blogosphere!
    Nice to see another Howler make the....well, whatever size of time this is ;-).
    (If you follow the link back to my blog, you may be able to figure out who I am)

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  4. Good job, that was a really clear and interesting explanation. It will be a pleasure to read more of these in the future!

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  5. Fascinating! Anonymous makes a good point, wouldn't the smaller ones have been preyed on by juvenile anomalocaris?

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  6. I loved the post! I hope to come back here regularly, as palaeoeverything is one of my favourite subjects.

    It has, however, been a long time since my own palaeozoology courses, and I was hoping you could clear up my confusion about one thing. You mention early on that you "[accept] natural selection as a powerful evolutionary mechanism, [but consider] that there are other, equally, or perhaps more, powerful mechanism out there, such as genetic drift". From there we have the fascinating case of the demise of Anomalocaris, as mediated by the developing ability of its prey to enroll themselves.

    It strikes me, however, that natural selection is still an adequate explanatory mechanism for the event in question. The selection pressure operating on the trilobites encouraged enrolling behaviour as an aid to molting, and in so doing, produced an exaptation which served as a stunningly effective defense against predation. In the context of a thorough understanding of this predator-prey interaction, the operation of natural selection on the prey species seems to provide sufficient explanation. Where do the other mechanisms driving evolutionary change come into play, in this case?

    Am I being overly reductive? Is this just an issue of semantics? I imagine things would be cleared up by reading the paper you've mentioned, but I probably won't be able to dive into it for a while. At any rate, thanks for joining the blog scene; I'm sure I'll be back many a time to get my palaeo-fix.

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  7. Nice post! Stopped by via PZ Myers' blog.

    " ... not everything that happens in evolution occurs because it was selected for."

    I thought that sounds "Gouldian"...until I saw the authors of that nicely named paper. I'll have to go and read it!

    " If the kids that burn the wings off insects had aquaria, this is what they’d want in it."

    Well, an anomalocaris would be too big for my aquarium, but I'd happily settle for an opabinia!

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  8. This comment has been removed by the author.

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  9. Hi Chris, another Kate here. Congrats on your new blog. I came via Pharyngula. Looks very interesting, I'll probably be back.

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  10. StridentLobster said

    It strikes me, however, that natural selection is still an adequate explanatory mechanism for the event in question.

    The post was against claims that evolutionary events occur because the traits that cause them are selected for to cause the event.

    The ability to defend against Anomalocaris did not evolve to defend against Anomalocaris but to assist moulting. Therefore there was no positive selection pressure to evolve the ability to enroll as a defence against Anomalocaris . The defence arose for other reasons unrelated to defence.

    Once present, the impact of the trait (demise of Anomalocaris) may have been selected for, but the evolution of the trait had nothing to do with Anomalocaris.

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  11. "... would draw attention to itself at a very venerable time"

    I think you mean vulnerable there.

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  12. The post was against claims that evolutionary events occur because the traits that cause them are selected for to cause the event.

    The ability to defend against Anomalocaris did not evolve to defend against Anomalocaris but to assist moulting. Therefore there was no positive selection pressure to evolve the ability to enroll as a defence against Anomalocaris . The defence arose for other reasons unrelated to defence.


    Yet, it's still natural selection, isn't it? It seems like just a standard case of exaption; the ability to roll evolved for one purpose (moulting) and was subsequently adopted for another (defense from predation)

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  13. Yet, it's still natural selection, isn't it? It seems like just a standard case of exaption; the ability to roll evolved for one purpose (moulting) and was subsequently adopted for another (defense from predation)

    Which is not a "straight" reading of how natural selection works, hence why it is covered in "other mechanisms". (Another Pharyngulite here. *waves tentacle*)

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  14. I disagree that enrolling in trilobites is an example of a spandrel. Gould's explanation was that a spandrel is a feature that is a structural byproduct of the evolution/development of some other feature. According to him there was no need to invoke natural selection to explain the origin of such byproducts. . I don't see a logical link between this and exaptation which is a change in functionality of a feature which previously served a different function and could have originally evolved through natural selection.

    Here clearly the origin of enrolling can be explained through natural selection. A change of functionality (exaptation) is fairly common in evolution. Including such examples as spandrels would make the definition too broad.

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  15. Which is why I said at the start:

    Here I’d like to develop that theme using Anomalocarus

    I've developed the theme further, and you are right, the definition is broad. But that's the point. There are so many examples that the purely adaptationist "programme" is untenable.

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  16. It's debatable if juvenile Anomalocaris ate trilobites. They probably did to a certain extent, but I suspect that baby Anomalocaris was not strong enough the break through the hard cuticle of trilobites until they got to a certain size. Plus there was a smorgasbourg of other small critters around to feed on.

    Once Anomalocairis got to a certain size, the menu became restricted to the larger trilobites as the only worthwhile meal.

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  17. Chris - I guess I am confused on why you treat enrollment in trilobites as a spandrel.

    Spandrels are byproducts of the evolution of some other feature. They are features which initially have no biological function.

    Now from your post I gather that you treat enrollment as an exaptation. But is it exaptation that arose through:

    a) co-option of an adaptation or

    b) co-option of a spandrel

    I think it is the former, the fortuitous use of the modified exoskeleton as predator defence is an exaptation that arose through co-option of an adaptation i.e. enrollement.

    Spandrels are accidents available for exaptation. In this case I don't see how enrollment can be considered as an accidental byproduct which was co-opted for predator defense.

    I think a lot of disagreements over these issues arise because of a conflation of the terms spandrel and exaptation.

    regards

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  18. Just wanted to drop by and say that I came across this place through the Self-Designed Student blog.

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  19. I'm wondering if there are any significant similarities between anomalocaris and animals in the order anostraca, the fairy shrimp.

    Also, the Ediacaran rocks! I want to hear more about the "quilted matress" animals if you would post about them.

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  20. But what (and how) ate the big trilobites after "Anomy" wasn't around and before jawed fish appeared? What is more powerful than Anomy's appendages?

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