Sunday, March 06, 2011

The Blue-footed Booby


The question of the week in New Scientist (Feb. 12-18, 2011) is, "The blue-footed booby is an extraordinary-looking bird. It has fairly dull plumage but strikingly coloured blue legs and feet. What could be the evolutionary benefit of such a conspicuous feature? Both sexes have blue feet so they don't seem to be for impressing potential mates."

This is bound to bring out the adaptationists. You can be almost certain that the answers will consist of various just-so stories based on the assumption that blue feet have to be an adaptation. Can you make up a good adaptationist story to explain the blue feet? It doesn't have to have any supporting evidence. Try and avoid explanations that rely on sexual selection—that's too easy.

The evolutionary relationship between the various booby species is shown below in a figure take from Friesen and Anderson (1997). The Peruvian and blue-footed boobies apparently diverged from a common ancestor about 200,000 years ago. The Blue-footed booby's range is northern Peru and the Peruvian booby lives in southern Peru. They do not form hybrids where their ranges overlap.



[Photo Credit: Wikipedia]

Friesen, V.L. and Abderson, D.J. (1997) Phylogeny and Evolution of the Sulidae (Aves: Pelecaniformes): A Test of Alternative Modes of Speciation. Molec. Phylo. Evol. 7:252-260 [doi:10.1006/mpev.1996.0397]

43 comments :

  1. Their feet are not blue. Their feet are mirrored, and you simply see the sky reflected in their mirrored feet.

    Natural Selection gave the Boobies mirrored feet as an adaptation and a perfected means of defense wherein they can appear to not be paying attention, and yet still be able to see predators while staring at their feet.

    Interestingly, the much-used ability of male Boobies to look up the skirts of female Boobies by simply staring at their own feet is a well-documented exaptation.

    Now what is my Boobie Prize?

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  2. Ancient predators were frightened of the color blue!

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  3. Hmm. I don't know enough about boobie life history to hazard a guess that is anything but facetious and the first comment may have already knocked that one out of the park. My first suggestion would be to do an experiment: paint the feet of unpaired boobies some other colours, compare to control boobies with blue painted feet, and perhaps another group with no paint at all, and see if changing the colour makes them unable to attract a mate or makes it take longer for them to do so.

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  4. I have a question. I live in Oregon. we have a mix of trees about my house, fir, oak and maple. The oak leaves are especially hard to blow off the driveway with a leaf blower. They just sit there is a full gale. The fir needles and maple (huge leaf maple) blow off easily.

    What evolutionary advantage do these oak leaves have to resist leaf blowing on pavement?

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  5. What's the difference between a just-so story and a hypothesis?

    (This is bound to make Larry say that it's shocking that I would have to ask such a question in 2011.)

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  6. I'd be willing to bet it is sexual selection. This is an hypothesis that should be easy to test, if one were so inclined.

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  7. Birds are tetrachromats, so who knows if they even find the blue vivid and outstanding in the same way we trichromat humans do? We may very well be giving a crap about something the birds themselves don't give a crap about.

    What's the difference between a just-so story and a hypothesis?

    The willingness to subject one but not the other to a test?

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  8. the blue foot is an adaptation for getting more food in the water. Fish or other water dwelling creatures do not suspect a bird ready to eat them since there is no color change from beneath the water.

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  9. There is a fairly robust body of literature on the role that foot pigmentation plays in both mate selection and parental investment in Blue-footed Boobies (a Google Scholar search for "Blue Footed Booby Foot" turns up many of the relevant papers). Whether you buy the results, or take them to tell you anything about the long-term origin and evolution of the trait is another matter. But it seems a bit silly that New Scientist is framing this as some vexing mystery, also to promulgate the myth that traits subject to sexual selection must be dimorphic. Another group of sea bird (alcids) have been my go-to counter example for this for a while.

    Larry's mention of the Peruvian Booby makes me wonder if he is thinking about mate recognition and sympatric speciation ... ?

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  10. Just FYI, the singular is booby (not boobie).

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  11. Obviously, it's for camouflage against the sky when they're flying ;-).

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  12. It's purpose was to inspire that well known Carl Perkin's Rock'n'Roll song:

    You can do anything
    When you beat your meat
    But please don't spray
    On my Blue Booby feet

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  13. Obviously those boobies are attracted to cold-hearted mates. To show their cold-heartedness through the colour of their feet is just the next logical step.

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  14. Scott says,

    Just FYI, the singular is booby (not boobie).

    Thanks. I changed everything in the posting.

    That was a test to see if anyone was paying attention. :-)

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  15. Bjørn Østman asks,

    What's the difference between a just-so story and a hypothesis?

    A scientific hypothesis generally follows the evidence, not proceeds it. In this case, the important question is "Are blue feet adaptive?"

    Once you have good evidence for, or against, adaptation you can start to narrow down the opinions by asking for even more evidence.

    For example, if you find that having blue feet actually confers a selective advantage on individual blue-footed boobies, then you can ask whether this is due to sexual selection or something else.

    Once you have some preliminary data, you can start to formulate an hypothesis that accounts for the data.

    Just-so stories often skip all these preliminaries and jump right to an explanation based on merely assuming that the data are obvious.

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  16. Try and avoid explanations that rely on sexual selection—that's too easy.

    Why? Sometimes the obviously correct answer is the factually correct answer.

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  17. anonymous says, concerning sexual selection,

    Why? Sometimes the obviously correct answer is the factually correct answer.

    I prefer asking questions about morphological differences between species of dandelions, mushrooms, protozoa, or bacteria.

    That's a convenient way to eliminate all those people who fall back on sexual selection when nothing else seems to work.

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  18. Blue does seem to be involved in sexual selection in other taxa. For example, there are Asian frogs living in swift streams where the white noise of rushing water would drown out vocalzations, males attract attention by waving blue feet apparently to attract females.

    Blue is also common in other birds, the dew laps of anole lizards, etc.

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  19. Neil, I've noticed the same thing in a lot of these new "gee wiz look at what we discovered papers". I remember when starting to do my PhD work nearly every question I had was answered ages ago by one long dead European (usually German) or another. Of course, I found this out by getting off my ass and going to the library and using indices that went back before 1980. It seems that some researchers think that nothing happened before electronic indexing!

    As for the adaptive nature of booby feet... damn that first commenter really did cover it nicely didn't (s)he?

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  20. Once you have some preliminary data, you can start to formulate an hypothesis that accounts for the data.

    

Just-so stories often skip all these preliminaries and jump right to an explanation based on merely assuming that the data are obvious.


    Larry, I think you're using this highly derogatory term "just-so story" too readily.

    Check out wikipedia:

    "A just-so story, also called the ad hoc fallacy, is a term used in academic anthropology, biological sciences, social sciences, and philosophy. It describes an unverifiable and unfalsifiable narrative explanation for a cultural practice, a biological trait, or behavior of humans or other animals. The use of the term is an implicit criticism that reminds the hearer of the essentially fictional and unprovable nature of such an explanation. Such tales are common in folklore and mythology (where they are known as etiological myths — see etiology).

    (…)

    The generation of plausible hypotheses is one part of theory creation and evaluation in normal science. The hypotheses are sufficiently plausible that they are taken seriously by experts in the field. Essentially, the key difference between a "just so story" and a scientific hypothesis is that the latter can be proven wrong, while the former cannot."

    Contrary to how you think about it, this way of looking at it makes a hypothesis a just-so story if no evidence can be gathered to refute/verify it. I really don't see why you would call a hypothesis a just-so story if people are explicitly doing nothing more than hypothesizing, rather than saying or it is actually so without (or despite) evidence.

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  21. That must be one hell of a paper. It was listed at $41.95 to purchase the pdf.

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  22. Larry-

    Do you have any evidence that the hypothesis that the coloration of the blue-footed booby feet is adaptive has not been tested adequately?

    I enjoy your questioning of adaptationism qua the assumption that every trait is adaptive, but your presentation here seems merely to assert that the hypothesis has not been demonstrated to be adaptive without presenting any evidence that the question of the adaptive value of the trait has not been tested against non-adaptive hypothesis.

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  23. Bjørn Østman says,

    Larry, I think you're using this highly derogatory term "just-so story" too readily.

    Check out wikipedia:

    "A just-so story, also called the ad hoc fallacy, is a term used in academic anthropology, biological sciences, social sciences, and philosophy. It describes an unverifiable and unfalsifiable narrative explanation for a cultural practice, a biological trait, or behavior of humans or other animals. The use of the term is an implicit criticism that reminds the hearer of the essentially fictional and unprovable nature of such an explanation. Such tales are common in folklore and mythology (where they are known as etiological myths — see etiology).


    That's an excellent description of a just-so story. I corresponds exactly to what I mean.

    Here's a ggod example of a Just-so Story. Here's another: How Women Got Their Menopause. And another: The Selective Advantages of Hairlessness, Baldness, and Gray Hair. And one more for good measure: Elaine Morgan and Aquatic Apes.

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  24. Michael M asks,

    Do you have any evidence that the hypothesis that the coloration of the blue-footed booby feet is adaptive has not been tested adequately?

    I read some of the papers that test whether blue feet confers an advantage due to sexual selection in current blue-footed boobies. I don't find the evidence convincing and I don't see how it explains the fixation of the blue-footed allele in some booby species and not in others.

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  25. I read some of the papers that test whether blue feet confers an advantage due to sexual selection in current blue-footed boobies. I don't find the evidence convincing and I don't see how it explains the fixation of the blue-footed allele in some booby species and not in others.

    Don't you think this says about you than the adaptive hypotheses?

    Can you provide an example of where you have spoken highly of an adaptive hypothesis on this blog?

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  26. I don't see how it explains the fixation of the blue-footed allele in some booby species and not in others.

    So why hasn't the gene for the blue-footed allele decayed to non-functionality through mutation then? Are you arguing there is non-sexual negative selection against disrupted alleles?

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  27. "Both sexes have blue feet so they don't seem to be for impressing potential mates"

    Non sequitur. A female with blue feet can be impressed by male blue feet. And vice versa.

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  28. Micahel M says,

    Don't you think this says about you than the adaptive hypotheses?

    Yes. That's the point. Different people have different perspectives of evolution and they will interpret data in different ways. I'm not really trying to convince you to be a pluralist—although that would be a nice bonus—I'm trying to convince you that adapationists have certain biases that influence the way they think about biology.

    Pluralists, by and large, are fully aware of the fact that science is a human endeavor. Adaptationists, on the other hand, usually fail to recognize that what they say about biology is often more a reflection of them than the science. They always seem to think it's the pluralists—not them—who are lettingt heir personal views get in the way of true science.

    One can continue to be an adaptationist if that's what one chooses. All I ask is that they recognize that this is a personal preferences (worldview) that's not necessarily the correct view. It's certainly not the only valid way to look at a problem.

    Can you provide an example of where you have spoken highly of an adaptive hypothesis on this blog?

    There are very, very, few. The good examples of adaptive hypotheses are boring and obvious so I don't blog about them. I'm much more interested in the controversial aspects of biology and evolution.

    I've got plenty of examples of adaptation and adaptive explanations in my textbook.

    Do you have any good examples of adaptive hypotheses that I should blog about?

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  29. anonymous asks,

    So why hasn't the gene for the blue-footed allele decayed to non-functionality through mutation then? Are you arguing there is non-sexual negative selection against disrupted alleles?

    Actually I not arguing in favor of any explanation for blue feet. I don't know if it's an adaption or not.

    The point of this blog posting was to show you how common adaptationist reasoning has become in biology. The mere suggestion that something as obvious as blue feet might not be adaptive is enough to bring out the adaptationist big guns.

    It's also a good example of the power of sexual selection as an adaptationist fall-back position.

    It's also important to recognize that there's a distinction between how a trait came to be fixed in a population and how it may be preserved once it has become fixed.

    It's possible that the allele for blue feet could have become fixed by accident just as the allele for red feet became fixed in the red-footed booby and the allele for gray feet became fixed in the Peruvian booby. However, once every booby had blue feet there may be a selection against those who have feet of another color because they look so different.

    Your question above seems to imply that fixation of any neutral allele is unstable because they should "decay to non-functionality through mutation." That misses the point. The blue foot allele is possibly non-functional to begin with (that's why it's neutral).

    The fixation of any neutral allele is a low probability event so it's loss is also a low probability event.

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  30. That's an excellent description of a just-so story. I corresponds exactly to what I mean. 

Here's a ggod example of a Just-so Story. Here's another: How Women Got Their Menopause. And another: The Selective Advantages of Hairlessness, Baldness, and Gray Hair. And one more for good measure: Elaine Morgan and Aquatic Apes.

    Really?! The way you present just-so stories above is about what the hypothesis is based on, not whether it is unfalsifiable.

    As for the Aquatic Ape, that one is definitely not unfalsifiable. I was talking with Daniel Dennett once about pet crazy theories, and I mentioned this one, to which Dennett replied that he actually believed in it, at least to the extent that he has never seen any data conclusively refuting it. Tim White was standing a few feet away, and we asked him what he thought, and he told us that if humans has gone through a phase living in an aquatic environment, then certain isotopes should be found in our bones (not sure about the details here), and they are not.

    As for blue feet: fixation by drift of the alleles responsible for making the feet blue seems unlikely. Selection would, in the least, make a good explanation for why the blueness doesn't degrade, as anonymous asks about. Therefore, making hypotheses (always fun) to explain how selection maintains the trait should not be so easily scoffed at, imo. As long as other hypotheses are entertained (such as drift) and a firm conclusion isn't reached without good evidence, I can see nothing wrong with it.

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  31. Bjørn Østman says,

    As for the Aquatic Ape, that one is definitely not unfalsifiable.

    Really? See Zombie Theories. The "beauty" of most just-so stories is that they have an intrinsic life of their own and can't ever be disproven. Of course they can't be proven either, but that doesn't seem important to the true believers.

    As for blue feet: fixation by drift of the alleles responsible for making the feet blue seems unlikely. Selection would, in the least, make a good explanation for why the blueness doesn't degrade, ...

    I don't get this. Why are neutral alleles supposed to degrade? Your proteins contain dozens of neutral amino acid substitutions that have become fixed in the hominid lineage since we diverged from our chimp cousins. Are you expecting them to "degrade"? What does that even mean?

    As long as other hypotheses are entertained (such as drift) and a firm conclusion isn't reached without good evidence, I can see nothing wrong with it.

    I agree. Under those conditions I see nothing wrong with speculations. I'm looking for a scientific paper that begins with ...

    "We are interested in how blue feet evolved in the blue-footed booby. We don't know whether the allele(s) are neutral and became fixed by random genetic drift or whether the blue foot allele confers some elective advantage. Let's imagine, for the sake of argument, that there's a selective advantage even though this has not been demonstrated. Here's a story that could explain such an adaptation. We recognize that there are many other, equally plausible, stories, including non-adaptive ones."

    Have you ever seen a paper like this?

    Why is it that you seem to be far more comfortable with speculations about adaptation than with speculations invoking random genetic drift?

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  32. “Actually I’m not arguing in favor of any explanation for blue feet. I don't know if it's an adaption or not.

    The point of this blog posting was to show you how common adaptationist reasoning has become in biology. The mere suggestion that something as obvious as blue feet might not be adaptive is enough to bring out the adaptationist big guns.”

    Translation:

    “I don’t actually believe this shit about neutral mutations, but I do enjoy playing Devil’s advocate and winding up Richard Dawkins.”

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  33. Really? See Zombie Theories. The "beauty" of most just-so stories is that they have an intrinsic life of their own and can't ever be disproven. Of course they can't be proven either, but that doesn't seem important to the true believers.

    I really don't care what Greg Laden has to say about the subject, Larry. Tim White gave a good reason to refute the theory. That crackpots refuse to see it is neither here nor there.

    I don't get this. Why are neutral alleles supposed to degrade? Your proteins contain dozens of neutral amino acid substitutions that have become fixed in the hominid lineage since we diverged from our chimp cousins. Are you expecting them to "degrade"? What does that even mean?

    But, you are confusing neutral substation in the gene with the function of the gene being neutral. Those aren't the same thing. Yes, many mutations do not alter the gene (killing it's ability to make blue pigment), so those mutations can drift to fixation (or if there are many mutations, make that gene behave like a quasi-species, of you will). If there is a set of genes that code for blue feet, and if these alleles are drifting, then eventually they would lose the ability to make the blue pigment. You say 'neutral alleles', but I say that alleles that make the feet blue has that specific function (this is of course all assuming there is no pleiotropic effects, which there could very well be), so they are not neutral. If there was no selection for blue, then offspring should be born with mutations in these genes that would degrade the function of the gene, and their new alleles would result in the same fitness, and non-blue feet would soon be prominent in the population.

    Have you ever seen a paper like this?

    No, I have not. Not only because the wording is rather pedestrian, but because there really is no need to say that neutral evolution could have done it, because that is the null hypothesis (should be in the minds of everyone): There is ALWAYS drift (except in the case of infinite populations), and selection is on top of that to varying degrees. Think about the selection coefficient - there is a smooth transition between the extremes of drift and very strong selection.

    Why is it that you seem to be far more comfortable with speculations about adaptation than with speculations invoking random genetic drift?

    Because selection can explain things that neutral evolution cannot. Blue-footed boobies is one example (assuming there is no linkage, and that they have been blue for a rather long time). Alleles that are fixed for long periods of time will degrade when mutations accumulate. To emphasize, I of course don't think there is selection on every individual codon, but if a protein has a function, then there will likely be selection for retaining that function (assuming that it has had it for a long time).

    It appears to me that I am the one of us who will entertain both kinds of hypotheses, whereas you have this innate dislike of adaptationist explanations (which I only dislike when people present them as truth without backing it up with data).

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  34. The fixation of any neutral allele is a low probability event so it's loss is also a low probability event.

    This is only true if the frequency of the allele in question is high and the number of generations is small. In fact, it is a bit disingenuous for you to claim the above, because the 2s approximation for the fixation of an allele, is derived from the limit behavior of the allele frequency distribution in infinite time, which has only two states "fixed" and "lost". The two-state nature of the limit behavior means that, if one calculates the probability of one of the states, one automatically and by definition has the probability of the other state. In other words, if the fixation probability of an allele is low the probability of its loss is high, contradicting your assertion that the probability of a neutral allele's being lost is low, at last in general and, more importantly, in the cases that are intersting to you.

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  35. Bjørn Østman says,

    If there was no selection for blue, then offspring should be born with mutations in these genes that would degrade the function of the gene, and their new alleles would result in the same fitness, and non-blue feet would soon be prominent in the population.

    It sounds like you're making a case for everything to be under selection. Otherwise it would have "degraded."

    I really don't understand where you're coming from on this. Are you saying that if the blue-foot allele really was neutral and really did become fixed in the population then it should be rapidly replaced by another neutral allele?

    Why?

    Because selection can explain things that neutral evolution cannot. Blue-footed boobies is one example (assuming there is no linkage, and that they have been blue for a rather long time). Alleles that are fixed for long periods of time will degrade when mutations accumulate.

    It's true that if the allele for blue feet isn't essential then the current allele could be replaced by an allele that doesn't encode blue feet. What I don't understand is why you think this is so probable an event that its absence suggests that selection is involved.

    It appears to me that I am the one of us who will entertain both kinds of hypotheses, whereas you have this innate dislike of adaptationist explanations ...

    I dislike most adaptationist explanations because they don't stand up to close scrutiny. They end up being just stories with no more evidence to support them than any other explanation—including non-adaptationist ones. Problem is, people end up believing the stories simply because they sound plausible and they fit with preconceptions about the importance of natural selection.

    When you don't know something the most scientific thing you can say is, "I don't know."

    I don't know why blue-footed boobies have blue feet. I don't know if it's an adaptation or not. What I do know is that none of the proposed explanations are convincing and I don't mind saying so.

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  36. Michael M says,

    In other words, if the fixation probability of an allele is low the probability of its loss is high, contradicting your assertion that the probability of a neutral allele's being lost is low, at last in general and, more importantly, in the cases that are intersting to you.

    I don't know if you are being ornery or if you really don't understand the issue.

    Let me try, once again, to explain it.

    Assume that the allele for blue feet is neutral. It became fixed in the blue-footed booby species by random genetic drift over a long period of time.

    We agree that the probability of fixation was low but it happened and we are now seeing the result. It's like meeting a lottery winner.

    If we agree that the probability of fixing a neutral allele is low then it's very unlikely that we are going to see the blue-foot allele replaced by another neutral allele—at least not very quickly. It's like recognizing that the lottery winner isn't very likely to win another big prize.

    You seem to be saying that if it's neutral the blue-foot allele should have degenerated.

    Maybe the the gray-footed allele in the ancestral population was neutral and it "degenerated" into the blue-footed allele. What do you think of that possibility? :-)

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  37. Blue feet are (surely, this is my assumption) made by a pigment. Assume there is no selection for having blue feet, and that a single allele (same argument for multiple alleles) is responsible for coding this pigment. This blue-allele could indeed have drifted to fixation, no question. However, given some time, mutations would accumulate, and at some point you would get some (e.g. stop codons) that would disrupt the protein, and the blue pigment would no longer be made. Since the trait of blue feet was neutral, there'd be nothing to stop feet with no color from appearing - offspring with gray feet (or whatever the colorless feet look like) would be just as fit, and there would be other non-blue alleles mixed with blue alleles in the population. Therefore, if there are no non-blue footed boobies in the blue-footed boobies population, then something else that neutral evolution is needed to explain the situation (selection, pleiotropy, linkage).

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  38. The easiest hyphotesis (at least for me) are sexual selection and "good genes": feet blueness is "attractive" in these boobies and /or an indicator of mate quality.
    These hypothesis have been experimentally tested:

    http://www.springerlink.com/content/917544751420697m/

    In the abstract:

    (...) In 48 h foot colour became duller when males were food deprived and brighter when they were re-fed with fresh fish. Variation of dietary carotenoids induced comparable changes in cell-mediated immune function and foot colour, suggesting that carotenoid-pigmentation reveals the immunological state of individuals. These results suggest that pigment-based foot colour is a rapid honest signal of current condition. In a second experiment, we found that rapid variation in male foot colour caused parallel variation in female reproductive investment. One day after the first egg was laid we captured the males and modified the foot colour of experimental males with a non-toxic and water resistant duller blue intensive make-up, mimicking males in low condition. Females decreased the size of their second eggs, relative to the second egg of control females, when the feet of their mates were experimentally duller. Since brood reduction in this species is related to size differences between brood mates at hatching, by laying lighter second eggs females are facilitating brood reduction. Our data indicate that blue-footed booby females are continuously evaluating their mates and can perform rapid adjustments of reproductive investment by using dynamic sexual traits.

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  39. "Blue feet are (surely, this is my assumption) made by a pigment."

    It seems to be a complex feature: structural based coloration due to collagen fibers, plus pigment. It has also ambiental influence (food makes the blue brighter quickly, malnutrition makes dull feet).

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  40. Bjørn Østman and El Paleo Freak-

    While it may be true that blue feet in the blue-footed booby are maintained by natural selection, Larry is talking about the original fixation of the trait. The fixation of a trait and its maintenance after fixation are two different phenomena; therefore, evidence that the trait is maintained by natural selection is not evidence that it was fixed by natural selection.

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  41. "Larry is talking about the original fixation of the trait"

    Well, in the post, he is talking about blue feet being an adaptation. And explanations that rely on sexual selection being "too easy".

    "evidence that the trait is maintained by natural selection is not evidence that it was fixed by natural selection"

    You are right. But here we have some evidence that the trait is adaptative *and* complex. It's hard to explain adaptative and complex traits with an initial random fixation of the whole trait (being probably generated by several genes) and subsequent selective maintenance of the same trait that, suddenly, becomes non neutral.

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  42. Bjørn Østman:
    "Since the trait of blue feet was neutral, there'd be nothing to stop feet with no color from appearing[...]and there would be other non-blue alleles mixed with blue alleles in the population."
    How would the blue-foot allele get to fixation if this is the case? Why wouldn't it be degrading while fixing, and thus never fix? Is there I difference? (I don't know, I'm asking, doesn't seem like there is, but maybe I don't understand).

    Dr. Moran:
    "Pluralists, by and large, are fully aware of the fact that science is a human endeavor. Adaptationists"
    So pluralists are like constructivists in the social sciences (they think theories aren't ever going to be perfect descriptions of nature, but that they're social constructs first and foremost).
    The constructivists (and a lot of the social sciences apparently) owe their origin to Marx's interpretation of history.
    So you're a Commie. I shoulda known!!
    You're upset that its not a pink footed wobbly booby!

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