Tuesday, June 26, 2007

Darwin Still Rules, but Some Biologists Dream of a Paradigm Shift

 
That's the title of an article in today's New York times. It's written by Douglas H. Erwin, "a senior scientist at the National Museum of Natural History at the Smithsonian Institution and a research professor at the Santa Fe Institute." You can read the entire article here.

Erwin says some rather silly things about "paradigm shifts" but I'll leave that to people like John Wilkins who know what Thomas Kuhn really meant. Suffice to say, the term is very much abused these days.

Putting that aside, Erwin makes some good points about the controversies in modern evolutionary theory. He points out that most of the old "paradigm" about evolution by natural selection is being challenged in one way or another. For example,
In the past few years every element of this paradigm has been attacked. Concerns about the sources of evolutionary innovation and discoveries about how DNA evolves have led some to propose that mutations, not selection, drive much of evolution, or at least the main episodes of innovation, like the origin of major animal groups, including vertebrates.
This is correct. There's a resurgence of "mutationism" that puts more emphasis on the role of mutation in evolution. This re-emphasis is not popular among evolutionary biologists but it's gaining ground.
Comparative studies of development have illuminated how genes operate, and evolve, and this places less emphasis on the gradual accumulation of small genetic changes emphasized by the modern synthesis. Work in ecology has emphasized the role organisms play in building their own environments, and studies of the fossil record raise questions about the role of competition. The last major challenge to the modern synthesis came in the 1970s and 1980s as my paleontological colleagues, including the late Stephen Jay Gould, argued for a hierarchical view of evolution, with selection occurring at many levels, including between species.
Again, these new ideas are all in play in modern evolutionary theory. The first refers to "evo-devo" and there's no question that some evolutionary biologists are rethinking evolution in light of the discoveries in developmental biology. (I think they're wrong, but that's not the point here.)

The last item refers to punctuated equilibria and hierarchical theory. There's little doubt that Gould's ideas have shaken up the old "paradigms."

I was disappointed that Erwin omitted the biggest threat to the old view of evolution, namely random genetic drift. While we've known about drift for decades the full scale of it's role in evolution is only now beginning to be appreciated. Most people still don't realize that random genetic drift is by far the most common mechanism of evolution.

[Hat Tip: Greg Laden]

21 comments :

  1. Not entirely knowing what a "paradigm shift" would entail, I can't agree or disagree with Dr. Erwin's main premise. I have, however, been among those who have argued that we need a "post-genomic evolutionary synthesis", an updated theoretical framework that expands on the "modern" (1930s and 40s) "synthesis" (of Mendelian inheritance and natural selection, but not of Fisher vs. Wright).

    We have learned a tremendous amount since the first half of the last century and it would be worth debating how all of this can be put together.

    I have focused on expanding the conception of mutation to include what we now know about genomics, and I and many others have written about natural selection as operating at multiple levels. Drift needs similar treatment, no question.

    Those broadened ideas, put together into a new and more comprehensive theory, would be the "post-genomic synthesis". (Incidentally, I have never proposed any "vague macroevolutionary mechanisms", despite what you may read in a recently released book; I propose the same principles we know -- mutation, selection, drift -- as applied to multiple levels and with more inclusive definitions that encompass post-1940s genetic discoveries).

    "Post-genomic", by the way, does not mean that only genomic information is playing a role -- it marks a particular moment in time (entry to the post-genomic era) as opposed to a nondescript label like "modern" or "neo".

    I am glad to see these issues being brought up.

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  2. Emphasize mutations all you want, but for evolution --an emergent property of populations--to occur, mutation has to be coupled with slelction and/or drift. Ehere's the new paradigm?

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  3. "random genetic drift is by far the most common mechanism of evolution"

    This statement may well be true at the levels of nucleotide-sequence changes and amino-acid changes, but I doubt it applies to the functional properties of proteins, let alone any higher level of phenotype.

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  4. Genetic drift is a real problem when you breed animals. You will find an example of what efforts it takes to cope with drift here:
    http://jaxmice.jax.org/geneticquality/stability.html

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  5. cpp says,

    This statement may well be true at the levels of nucleotide-sequence changes and amino-acid changes, but I doubt it applies to the functional properties of proteins, let alone any higher level of phenotype.

    Do you have a definition of evolution where my statement would be incorrect?

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  6. cpp asks,

    Emphasize mutations all you want, but for evolution --an emergent property of populations--to occur, mutation has to be coupled with slelction and/or drift. Ehere's the new paradigm?

    I don't like the word paradigm so I won't use it.

    The old way of thinking about evolution imagines that mutations are abundant so whenever an adaptation is needed it will occur with only a short delay. This is the Dawkins version of evolution with arms races and rapid adaptation to new environements etc.

    One of the newer ways of thinking about evolution is to imagine that the direction of evolution is determined in large part by the accidental availability of mutations that just happen to occur. It's not necessarily true that a required mutation will always be available when the environment changes. Sometimes the antelopes really will outrun the cheetahs and the cheetahs will become extinct before they can adapt.

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  7. The nice thing about Erwin's piece was that it contextualized the call for "paradigm shifts" and revolution rather than just beating the war drums for or against (which is what you usually get). And I think he pretty much made the right conclusion, which is that there is a lot of exciting new stuff, but it's too early to tell if it "really" is a revolution or more just evolution of the standard views.

    Unfortunately Erwin in one sentence perpetuated the idea that Nilsson & Pelger 1994 was a paper that did a computer simulation of eye evolution -- actually it was a mathematical model. Erwin got this mistake from Dawkins who spread it far and wide. The IDists jumped on this a few years ago but they seem to be missing the boat today...

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  8. I would guess that the possibility of directional selection and its actual direction could sometimes be a matter of what mutations happen to be there and at other times be like what you call the older model. This could depend on a number of things including what exactly has to happen for a certain directional shift to occur.

    Sometimes the baby is the bathwater. Sometimes it is not.

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  9. One of the newer ways of thinking about evolution is to imagine that the direction of evolution is determined in large part by the accidental availability of mutations that just happen to occur.

    This is new? I've been studying evolution as an interested nonscientist for a dozen years or more, and I can't recall ever thinking about evolution any other way. Certainly not after I read David Raup's perfectly-titled book Extinction: Bad Genes or Bad Luck?. It's the primary way that randomness works into the process: what genetic variants are available at any given time to meet any given selective influence?

    For that matter, I also realized early on that it's a mistake to talk only about "genetic mutations" as the fuel for evolutionary change when one actually means "genetic variations." Mutation and drift are just two of several known mechanisms that produce genetic variations. All such mechanisms are equally important, and anyone who tries to argue that this one or that one is the primary mechanism is getting away from the evidence.

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  10. "Do you have a definition of evolution where my statement would be incorrect?"

    "evolution is the change in the inherited traits of a population from generation to generation"

    From Wikipedia, but still...if "traits" means phenotypic traits (as it does, I think, to most biologists) then I suspect (without data) that drift is less important than selection in that context. A reductionist modern-synthesis definition of evolution as changes in gene frequencies makes good sense from the standpoint of population genetics, but it's not much help to a paleontologist or a physiologist, people who study phenotypes.

    Which is not to say that selection is unconstrained! Genetic variation is randomly generated, and (as pointwed out in comments above) the right mutation has to occur in the right place and time before selection (or, for that matter, drift) can even get started.

    I think there are lots of organisms that are better adapted to environments of the past than they are to their current circumstances (evolutionary psychologists would say the humans are examples)--it's the reason that rapid global climate change worries wildlife biologists.

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  11. Are rumors of the death of selection exaggerated?
    one indication ...
    http://www.pnas.org/cgi/content/abstract/104/16/6504?ck=nck

    Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila

    Stanley A. Sawyer, John Parsch, Zhi Zhang, and Daniel L. Hartl

    Abstract: We have estimated the selective effects of amino acid replacements in natural populations by comparing levels of polymorphism in 91 genes in African populations of Drosophila melanogaster with their divergence from Drosophila simulans. The genes include about equal numbers whose level of expression in adults is greater in males, greater in females, or approximately equal in the sexes. Markov chain Monte Carlo methods were used to sample key parameters in the stationary distribution of polymorphism and divergence in a model in which the selective effect of each nonsynonymous mutation is regarded as a random sample from some underlying normal distribution whose mean may differ from one gene to the next. Our analysis suggests that {approx}95% of all nonsynonymous mutations that could contribute to polymorphism or divergence are deleterious, and that the average proportion of deleterious amino acid polymorphisms in samples is {approx}70%. On the other hand, {approx}95% of fixed differences between species are positively selected, although the scaled selection coefficient (Nes) is very small. We estimate that {approx}46% of amino acid replacements have Nes < 2, {approx}84% have Nes < 4, and {approx}99% have Nes < 7. Although positive selection among amino acid differences between species seems pervasive, most of the selective effects could be regarded as nearly neutral. There are significant differences in selection between sex-biased and unbiased genes, which relate primarily to the mean of the distributions of mutational effects and the fraction of slightly deleterious and weakly beneficial mutations that are fixed.


    Carping about the modern synthesis:

    First the synthesis is defined in a certain way, with time and content restrictions.
    Then it is criticized for these restrictions.
    This game could also be played with physics or any other part of science. Happily, it is not. People recognize that the river of research flows ever faster and gains more tributaries. But for arbitrary time definitions, the Modern Synthesis never stopped being synthesized.

    Mutationism: The idea that mutations of large effect are significant in evolution. Hopeful monsters? No, large effect is > 8% in some measurable character.
    Who wins? As far as I know, it's a tie. Fewer mutations of large effect are influential in evolution, but they have more effect per capita.

    Pete Dunkelberg

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  12. While we've known about drift for decades the full scale of it's role in evolution is only now beginning to be appreciated. Most people still don't realize that random genetic drift is by far the most common mechanism of evolution.

    Sewall Wright was beating this drum back in the '30s. maybe drift is only beginning to be appreciated now in some parts of the biology world, but evolutionary biology isn't (or shouldn't be) one of them.

    in any case, the article in question was about phenotypic, not molecular, evolution, where neutral drift has a less important role-- even gene expression (possibly the noisiest phenotype?) evolves, as a general rule, under stringent stabilizing selection.

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  13. I was disappointed that Erwin omitted the biggest threat to the old view of evolution, namely random genetic drift. While we've known about drift for decades the full scale of it's role in evolution is only now beginning to be appreciated. Most people still don't realize that random genetic drift is by far the most common mechanism of evolution.

    I'm glad you pointed this out. Now if we could figure out how important genetic draft is....

    [/delurk]

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  14. p-ter says,

    Sewall Wright was beating this drum back in the '30s. maybe drift is only beginning to be appreciated now in some parts of the biology world, but evolutionary biology isn't (or shouldn't be) one of them.

    I agree that evolutionary biologists like Dawkins and the other adaptationists should have known about random genetic drift. Isn't it amazing that they don't?

    in any case, the article in question was about phenotypic, not molecular, evolution, where neutral drift has a less important role--

    Why do you say that? It's exactly the sort of attitude that I was complaining about when I said that drift isn't appreciated. The adaptationists dismiss it because they think, incorrectly, that it has nothing to do with "phenotypes." Lots of phenotypic changes are fixed by random genetic drift.

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  15. Lots of phenotypic changes are fixed by random genetic drift.

    Which always leads to the question:

    Where's the list, and the evidence?

    The first answer is that anyone who even asks must be a demented panadaptationist. But after that, where's the beef?

    Pete Dunkelberg

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  16. "Lots of phenotypic changes are fixed by random genetic drift."

    I'm with Pete on this one...evidence?
    I accede to the notion that adaptation should not be assumed without evidence (incidentally, Gould and Lewontin were not the first to emphasize this; GC Williams referred to adaptation as an "onerous" concept back in 1966).
    But doesn't evolution by random drift require similar documentation? Ignorance of responsible selection pressures (if any) (as is the case in many, if not most examples of phenotypic traits) does not mean that drift is responsible, just that we don't know. In most cases, we probably never will. (This is the reason for the "current utility" criterion of adaptation, which I deplore, by the way).

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  17. I agree that evolutionary biologists like Dawkins and the other adaptationists should have known about random genetic drift. Isn't it amazing that they don't?

    but of course they know about genetic drift. (it gets mentioned here, for example). it's true dawkins, for example, talks less about it, (as did R.A Fisher, as well) but that's an entirely different point.

    Lots of phenotypic changes are fixed by random genetic drift.

    it does stands to reason that if 70% of amino acid changes are not fixed by positive selection (as is estimated in drosophila), they should have some phenotypic effect. but then again, if they're neutral, maybe not. I can't think of a study of a higher-level phenotype that demonstrated lack of selective constraint (above I cited a study of gene expression, a fairly low-level phenotype, which demonstrated strong stabilizing selection. those sorts of experiments have been done in many organisms, with similar results). I'm of course open to being corrected on this point.

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  18. For examples of phenotypic changes that do not appear to be under selection, you need look no further than Homo sapiens. The common textbook examples are the ability to taste phenylthiocarbamide (PTC), blood types, tongue rolling, and eye color.

    In most other cases, the absence of selection is inferred rather than directly demonstrated so, strictly speaking, I should qualify the statement by saying that it's extremely likely that many phenotypic changes are fixed by random genetic drift.

    However, I don't see the same qualifiers on the other side where it is generally assumed—without any evidence whatsoever—that all phenotypic changes are fixed by natural selection.

    It's very likely that most of the the features that distinguish one race of humans from another are not adaptations. Does anyone want to argue that they are?

    At some point in the future all humans will probably resemble the average Asian. Will our descendants be silly enough to argue that all these features were selected?

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  19. The common textbook examples are the ability to taste phenylthiocarbamide (PTC), blood types, tongue rolling, and eye color

    hm, I'm not so sure. ability to taste PTC is almost certainly under natural selection. then there's the theory that eye color diversity was the result of frequency-dependant selection. It'll be interesting to look at the sequences around OCA2 in a number of individuals to see if there's a signature of selection. and about tongue-rolling, it certainly doesn't seem likely to confer any advantage, but I'm not ruling it out.

    It's very likely that most of the the features that distinguish one race of humans from another are not adaptations. Does anyone want to argue that they are?

    depends on what you mean by "most". At present, I'd argue most of the visible ones are indeed the result of natural selection. there's a lot of work on this right now (with the hapmap and whatnot). Nick Wade just had a great article on some of that work, or search my site for "recent evolution".

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  20. I see where you're coming from. You prefer to think of everything visible as an adaptation unless it can be proven otherwise. Because that's your personal bias, you tend to make a huge distinction between the vast majority of alleles at the molecular level and the subset that manifest themselves as a "visible" phenotype.

    I find this view difficult to understand. What is it about "visible" mutations that make them all subject to either negative or positive selection? Why can't visible mutations be neutral just like most other mutations?

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  21. What is it about "visible" mutations that make them all subject to either negative or positive selection? Why can't visible mutations be neutral just like most other mutations?

    well, selection acts on phenotype, not on genotype. so any "invisible" mutation absolutely cannot be acted upon by selection, whereas any "visible" mutation is, in principle, subject to selection. the only major pararameters are the selection coefficient (which could, of course, be 0) and the population size.

    this might be a personal bias in some situations, but with regards to human races, this is no longer empty theorizing-- it's an empirical question. Scans for selection based on exptensive genotyping in the major continental races pick up genes for skin color, bone morphology, hair morphology, etc. So are *all* the major differences between races the result of selection? Hard to tell. But many of them absolutely are-- don't let your a priori preference for neutrality (a defensible preference, of course) blind you to the data.

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