How do new kinds of bodies evolve? It's a question that obsesses many scientists today, as it has for decades. Yesterday, Olivia Judson, an evolutionary biologist and book author, published a blog post entitled "The Monster is Back, and It's Hopeful," in which she declared that these transitions can happen in sudden steps.
Even before I had finished reading Judson's piece, I got an email from the prominent evolutionary biologist Jerry Coyne grousing about it. Coyne, who teaches at the University of Chicago, is an expert on the genetics of adaptation as well as the origin of new species. He has written potent, eloquent attacks on creationism in places like the New Republic (pdf). Recently he has also begun to express skepticism about the grander claims for evolutionary developmental biology--"evo-devo" for short (see this pdf for more).
I thought it would be interesting to hear what Coyne had to say--at length. Since he does not (yet) have a blog of his own, I invited him to write a guest post for The Loom. He kindly sent in the following piece, which appears below the fold, entitled "Hopeless Monsters." Please give Dr. Coyne a warm welcome to world of science blogging, and let him know what you think in the comment thread.
(I'm posting this at about 11 am EST without links. This afternoon I should have enough free time to add links in. So if you want to follow up on this essay, come back.) Update: Links are in.
HOPELESS MONSTERS, by Jerry Coyne
Macromutationism is the idea that important evolutionary changes between groups were produced by single mutations with very large effects. Advocates of this idea propose that these mutations produce, in one fell swoop, complete new features that distinguish major groups, such as the extra pair of wings in dragonflies, the jaws of vertebrates, or the feathers of proto-birds. The first mutants with these new traits are famously known as "hopeful monsters."
The notion of macromutationism pops up every few years in evolutionary biology. It's wrong but it's resilient. It's like one of those large, roly-poly rubber clowns that I played with as a child: knock it down and it pops right back up again. The harder you knock it down, the faster it pops back up. First broached by the "mutationists" in the early twentieth century, and made famous by Richard Goldschmidt, the idea was batted down by, among others, Dobzhansky, Mayr, and many luminaries of the Modern Synthesis. The idea of macromutational hopeful monsters, or "saltations," had a prominent resurrection in 1980 when Stephen Jay Gould, as part of his and Niles Eldredge's theory of punctuated equilibrium, proposed that macromutations could explain the "jumps" in the fossil record. After getting a severe drubbing from geneticists, Eldredge and Gould retreated in 1993, claiming that they never suggested the idea of saltations. More recently, hopeful monsters have reared their heads from the land of evolutionary developmental biology ("evo devo"), some of whose advocates say that key regulatory mutations could lead to changes in the "Bauplan"--the basic anatomical structure of a major group. This notion, too, is controversial.
The issue remains alive because evolution is a historical science. The changes we are interested in happened in the distant past and they're very difficult to study. After all, it's hard to determine what genetic changes underlie the difference between, say, insects and crustaceans. The classical technique for figuring this out--using genetic crosses between the species to pin down the genes--is impossible between distantly related forms. You can try to cross a lobster with a butterfly but, be warned, it's going to be an unrewarding experience. Transgenic work may eventually solve the problem, but for now there's simply no evidence that macromutations have played a macro role in macroevolution.
But you wouldn't know this from Olivia Judson's Jan 22 posting on her New York Times blog, "The Wild Side." In her piece, called "The Monster is Back, and It's Hopeful," Judson pulls out all the stops trying to convince her readers that hopeful monsters are, after all, an entirely plausible--if not common--feature of evolution. She claims that "the idea of the hopeful monster has begun to stage a comeback."
Unfortunately, her piece is inaccurate and irresponsible, especially for a journalist with a strong science background (Judson has a doctorate from Oxford). I've admired Judson's columns and her whimsical and informative book Dr. Tatiana's Sex Advice to All Creation. But this latest posting is simply silly. As an evolutionary biologist, I'm used to seeing our field twisted out of shape to satisfy the demands of journalists who love sensational new findings--especially if they go against long-held Darwinian beliefs like the primacy of gradual, stepwise evolution. But I'm not used to seeing one of my own colleagues whip up excitement about evolutionary biology by distorting its findings.
How does Judson justify her enthusiasm for saltation? Just the facts, ma'am: it's supposedly due to new evidence. She notes, "The reason for the comeback is that some of the big changes in morphology that we see appear to be underpinned by changes to single genes." But when you look at the "evidence" she gives, the conclusion falls apart.
Judson commits two errors of reasoning when arguing a la Goldschmidt (or Gould). The first is what I call the "macromutationist fallacy," for this error is so common that it deserves a name. It is this: we see some single mutations within species that make big changes in a trait, and then infer that differences between species in that same trait are also due to mutations in that same gene, or to other mutations of large effect. Judson makes this mistake when discussing the naked head of the vulture, presumably an adaptation for sticking its noggin into rotten meat. She thinks that the loss of vulture head feathers may well be due to a single mutation because there are occasional mutations in domestic chickens that give them bare heads and necks.
But you can't blithely extrapolate from rare large-effect mutations within species, especially domesticated ones, to mutations causing large evolutionary changes between species. These macromutations, like those producing bald chickens, almost always have highly deleterious side effects that make them unlikely to form the basis for evolution in nature. In fact, many cultivated species would never survive, much less take over, in the wild. Domestic corn is good to eat, but would never thrive in nature because the seeds don't disperse. Or, take single mutations having drastic effects on body size. One of these, achondroplastic dwarfism in humans, has severe negative effects on health and reproduction. Saying that the bald-chicken mutation implies that vultures lost their top feathers courtesy of a single mutation is like saying that because there is dwarfism in humans, the size difference between humans and chimps must have the same genetic basis as achrondroplasty. Most big-effect mutations that occur in the laboratory, greenhouse, or henhouse could never survive in nature, and have to be coddled by humans to survive.
Judson's other error is especially common in the evo devo community. And that is assuming that if a change in gene expression is correlated with an evolutionary feature, then that change in gene expression must have caused that evolutionary feature. Judson cites a recent paper by Barmina and Kopp on sex combs in Drosophila species (these are clumps of stiff bristles on the foreleg of males that they use to grab females when mounting them). What Barmina and Kopp showed is that the expression of the Sex combs reduced (Scr) gene is correlated with whether or not males of a species have sex combs. In species whose males have sex combs, Scr expression is high in that sex and lower in females. When they don't have the combs, Scr expression is low in both sexes.
Judson interprets this as meaning that "the difference [in presence of sex combs between species] seems to be entirely due to changes in the way that a single gene, Sex combs reduced, is expressed in the front legs of the developing adult."
But it doesn't mean that at all. What it means is that Scr expression is associated with the difference in presence of sex combs. It does not mean that mutations in Scr suddenly produced sex combs. Scr could have some evolutionary role in the appearance of this trait, or it could have a negligible one. The occurrence of many small mutations in genes that control Scr expression is an equally plausible explanation for Barmino and Kopp's observation. In fact, the relevant scientific literature (which Judson fails to cite) shows just this--differences between species in sex comb size tend to be due to several to many genes of minor effect, most of them nowhere near the Scr locus.
Finally, Judson implies that changes in the Ultrabithorax (Ubx) gene between shrimp and Drosophila is responsible for the difference in leg number between crustaceans and insects. This experiment was done by inserting part of the shrimp Ubx gene into fly embryos. But when the researchers did this, they did not find that the shrimp gene suddenly allowed the flies to produce many new legs. Instead, the gene simply changed the expression of a few larval genes in a leg-like direction. There's no evidence at all that mutations in the Ultrabithorax gene were solely responsible--or even largely responsible--for the difference in leg number between crustaceans and flies. To know that, you'd have to either do genetic mapping between shrimp and flies that involves crossing them (impossible, of course), or show that the gene transplanted from shrimp to flies gives the flies many legs (and there's no evidence for that).
One of the authors of the Ultrabithorax study happens to be Sean Carroll, a prominent and respected advocate of evo devo. Yet Carroll utterly rejects the idea of saltation. As he says in his recent book, Endless Forms Most Beautiful, "For half a century since the Modern Synthesis, this specter of a 'hopeful monster' has lingered. The facts of Evo Devo squash it."
It's time to stop inferring how evolution works by simply extrapolating from mutations in the laboratory and henhouse and from correlations between gene expression patterns and appearance of new features. The way to find out what kinds of genes have caused evolutionary change is simply to do genetics.
Amidst the chorus of approbation that followed Judson's article (see the hundred-odd comments on her blog), I sound a dissenting note. Yes, it's important to educate the public about what's going on in evolutionary biology, but a scientist (if not a journalist) has a responsibility to describe the field accurately, caveats and all. If "the idea of the hopeful monster has begun to stage a comeback," it's done so only in Judson's mind.
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The idea of a 'hopeful monster' is appealing, and you explain very clearly why it is extremely unlikely. However, it comes across as something that is very extremely unlikely, but not actually impossible. I think that 'not actually impossible' is a lot of why the idea keeps coming back up.
(I had not thought that 'hopeful monsters' played any role in punctuated equilibrium, I thought that 'pe' was simply the observation that species at the edge of their range have slightly different selection pressures than in the middle of their range, and that if that 'edge population' becomes reproductively isolated it can speciate. Which always seemed pretty straight-forward to me.)
I don't think even the most strident evo-devotee, or Gould himself for that matter, would be very sympathetic to Judson's "just-so" arm waving. And it would be foolish to argue with the fact that classical genetics remains one of the most quantitatively rigorously avenues for investigating the nuts-and-bolts of evolution.
I think it goes to far to however to suggest that genetics is the ONLY valid avenue for investigating the nature of evolution, in the same way that it would be silly to say that particle physics is the only valid way to investigate the nature of the universe (though some particle physicists may hold that position). Quantum electrodynamics is not a very helpful tool when you want to calculate planetary orbits, and evolutionary theory without developmental biology, ecology or paleontology is, to misquote Einstein, blind, deaf and dumb.
I also thing it is unfair to chalk up PE as simple Goldschmidt retread. There are important differences between genetically based allopatric speciation on "rapid" thousand year timescales and sprouting wings overnight.
Likewise, before we write off any possibility of gaining evolutionary insight from the henhouse or the greenhouse, it's worth remembering the important role that hanging out with pigeon breeders played for Darwin developing his (limited) understanding of heredity in the days before Punnett Squares and Hardy-Weinberg. Co-evolution isn't restricted to the lab or the barnyard and deleterious side-effects may be the rule rather than the exception in important "natural" cases like sexual selection and eusociality.
One problem in terminology is that both fairly trivial changes, such as loss of feathers, and major topological changes, such as dorsal-ventral inversion, somehow fall under the rubric of "macromutation."
That aside, since I'm a "big tent evolutionist," let me suggest that both Fisher and Goldschmidt were right. Fisher was right that the larger the phenotypic effect of the mutation the more likely it is to be deleterious. But perhaps Goldschmidt was also right that non-deleterious macromutations are important in producing major innovations and higher taxa formation. A beneficial macromutation is similar to Nassim Taleb's concept of a Black Swan, a very improbable but very significant event.
I think Jerry Coyne might perhaps be committing what one might call the "inductive/probabilistic fallacy" -- if it doesn't happen much and there isn't a high chance of it, it cannot have and will not happen! ;-) This despite the escape clauses ("one cannot blithely...", etc).
I wonder if he will be "responsible" and back-up "accurately" his attacks on Gould (and others)... I won't hold my breath.
Just two comments
1. Re neil's comment: I didn't say that doing genetics was the only way to "investigate the nature of evolution." Rather, I said that it's really the only way to find out what GENES were involved in evoutionary change. I can't think of any other way to do this besides crossing species (impossible between distant relatives) or doing transgenics. If anybody knows another way, I'd be glad to hear it.
2. The original incarnation of punctuated equilibriumwas made more than just a claim of rapid allopatric speciation. The theory explicitly invoked instantaneous macromutational change. Here is a quote from Gould (1980, Paleobiology 6:119):
"I envisage a potential saltational origin for the essential features of key adaptations. Why may we not imagine that gill arch bones of an ancestral agnathan moved forward in one step to surround the mouth and form proto-jaws."
To me, this seems like a pretty big saltational change! Gould and Eldrdge later backed off on this, saying that "Opponents now accept that punctuated equilibrium was never meant as a saltational theory . . " (Gould and Eldredge Nature 366:326).
The problem I think, is that Gould and Eldredge were contantly changing the mixture of claims that constituted punctuated equilibrium, particularly those claims dealing with its mechanism. Brian Charlesworth and I discussed the constantly-morphing nature of punc. eq. in a letter to Science (1997 276:339-341; see also Gould and Eldredge's response on pp. 338-339 of the same issue).
I am quite certain that Gould and Eldredge did not backtrack from their hypothesis of punctuated equilibrium. If so, I would like to see some reference from them to this effect. And evolution is not 100% dependent on genetics. There can be evolutionary change in the absence of genetic involvement as Gilbert Gottlieb has pointed out.
I think it's safe to say that Gould sometimes presents a moving target. Gould aside, does anyone else wish to defend the proposal that true saltationism has a significant role in macroevolution?
(No, not an exclusive nor predominant role, as a certain Goldschmidtian blogger/commenter posits.)
Can't argue with that one!
Jerry Coyne responds:
I am not sure to whom this response is intended -- if it is intended to answer my call for Jerry Coyne to display the same responsibility he calls for in others, I am afraid it falls quite short, for it offers little to justify the spirit of statements such as:
(and that is one example).
To address the text from Coyne quoted above, note that Gould writes:
It is also worthy of note that Gould's text above [unintentionally] anticipates Coyne's demands for burden of proof i.e., who can blithely claim what.
That Gould can "envisage a potential saltational origin" does not commit "punctuated equilibrium" to be a "meant as a saltation theory".
Jerry: I'm sure you're right about everything you say (except the part about the chickens, see here. ). But a little harsh, aren't we?
"She thinks that the loss of vulture head feathers may well be [...]"
"But you can't blithely extrapolate from rare large-effect mutations within species [...]"
You can indeed blithely extrapolate when speaking in "may well be" mode - in other words, while brainstorming hypotheses. Dr Judson expressed considerable uncertainty about whether a single saltation actually denuded the vulture's head.
I guess the vulture idea may not contribute very much support to Dr Judson's suggestion that the hopeful monster doctrine is currently resurgent, since it's merely an idea, by Dr Judson's own admission. But at least she was clear about it being just an idea.
Overall, Dr Judson's essay seems to be quite far from suggesting that the existence of any mutant phenotype in any taxon proves, or strongly implies, that any similar phenotype that's fixed in any other taxon must have arisen as a saltation. Whereas Dr Coyne's essay, perhaps mostly by accident, seems overall to incorrectly attribute to Judson this position - a position which I don't think anyone would want to be associated with.
More importantly, it seems Dr Coyne may have refuted Judson's understanding of the ultrabithorax and sex comb stuff. Assuming so, I'm glad that was pointed out, and am grateful for Dr Coyne's piece.
I sincerely hope that the Texas Citizens for Science do not get a hold of this quote:
Mutations with large effects are not restricted to artificially selected breeds, but are also observed in the wild and in speciation processes. Consider melanism. or pelvic fin reduction in gasterosteus; or armor reduction in gasterosteus . Those are some pretty drastic morphological changes, documented by a few alleles with great effects, and it seems to me that Coyne is just glossing over the cases that do not fit his gradualism. His obviously sees restrictions to mutations with large effects that are unrealistic.
As a paleobiologist, I myself have in mind several lineages in the evolution of life that show changes such as homeotic transformations, hometic frameshifts, and other that are clearly qualitative, not fitting any gradualistic story. So my mind is pretty much made up, and I sort of smile at the "demonization" of saltationism.
I think the datum of the naked necks of african chickens mentioned by Greg laden clears up THAT case pretty well. This whole thing about the "horrific side effects" put forward by gradualists is always very speculative and adaptationist, based on mere correlations but rarely any actual mechanism. The naked neck of vultures being the result of a single mutation is a completely plausible hypothesis.
Those african chickens are probably one more of several documented cases of big differences in WILD populations. Usually it is a matter of a single or a few alleles; such as the melanism in Biston, for instance. This was no fading of several genes with small effect going to grey then black. It was....well, a MUTANT. With a DRASTIC effect on pigmentation.
The whole domestic vs wild argument of Mr. Coyne is completely unconvincing.
I would very much like to know what case would Mr. Coyne consider the best case study of the microevolutionary origin of an adaptation by gradual accumulation of several genes. Allen Orr, another expert on the genetics of adaptation, thinks that the documentation for this is lacking, whereas cases of single or few genes with large effects are much more common.
An auspicious and engaging blogging debut! A lot going on here, including a perennial tension found in both science and writing about science: The attraction to the attractive narrative on one hand and a commitment to rigor and what scientists call parsimony (the more simpler, more spare, more cautious explanation) on the other.
I once heard this expressed this way: At a table full of scientists and scientist types (groupies?), someone quoted Ptolemy (perhaps apocryphally; I can't find it anywhere):
"The goal of science is finding the most compelling story consistent with the facts."
Someone else at the table said,
"No! It is finding the simplest story consistent with the facts."
Betwixt lies all sorts of room for disagreement, including, it seems, this one. I'm not saying both Coyne and Judson are consistent with the facts on this one. (I'm no qualified judge, but Coyne convinces me Judson wandered astray.) But you see that tension here -- and elsewhere, constantly. In the pivotal 19th-century argument over evolution, for instance, which pitted two beautiful, compelling narratives against one another: Louis Agassiz's creationist yarn, which was a gorgeous narrative, and Charles Darwin's story of evolution by natural selection, which also had a great narrative drive (if no teleological 'motive') and a compelling aesthetic unity. Darwin's won out, of course (well, mostly ...) because he proved his more consistent with the facts.
But the same tension was at play. We find attractive narrative explanations that are simple -- but not TOO simple. And we like NOVEL things (or apparently novel things). This affects both scientists and scientific journalists. I would say, by the way, that sci journalists, just like others, DO have an obligation to describe a field accurately. Doesn't mean they can't go out on a limb with their own opinion or reading of something, though, as long as they make clear that -- and not reporting -- is what they're doing. This has its dangers, of course, which Judson has encountered in Coyne's post.
Thanks to Coyne for writing this and Carl for putting it up there.
David Dobbs
Contributor, NY Times Magazine and others
blog at Smooth Pebbles
Professor Coyne is right to chide Dr. Judson (NYT 22 Jan posting). However, he goes too far in equating Goldschmidt's hopeful monsters with Goldschmidt's macromutation concept as set out in his 1940 book. "Hopeful monsters" was a mere aside. Having dealt with micromutations in the first part of his book, Goldschmidt proposed a progressive cumulative mutational process occurring at the genome level that could lead to change in an organisms "reaction system." This macromutation was something occurring at the level of whole chromosomes or whole genomes that would allow rapid evolutionary advance (e.g. speciation). As examples of different reaction systems he pointed to the non-recombining parts of sex chromosomes, and the non-recombination of two genomes occupying the same nucleus (allopolyploids). At that time he could not be more specific since the structure of DNA was unknown. Modern bioinformatic analyses of genomes suggest that a change in "reaction system" can be equated with a change in the base composition "accent" of DNA.
Vultures also have long necks as well as bald ones. Is anyone suggesting that the two are unrelated? Did an ancestral vulture develop a long neck for reaching into the thoracic cavity of a dead zebra BEFORE losing its head feathers? There is no cost to losing head feathers that I can see at first sight. It can hardly count as a hopeful monster unless there is some fitness cost, surely, outweighed by the new development.
I am not aware of vulture development to know whether their headfeathers grow at first, are stunted, fall out, or progressively fall out as they feed on carcasses.
The flounder is an interesting issue. An eye progressing towards the (new) dorsum is of no advantage until it 'rounds the corner'. Whence comes the selection pressure for this gradual movement?
Matadors wave a red cape to enrage a bull, who then charges the cape - ultimately to his doom. In the same fashion there are lightning rod issues that cause humans to charge out.
In this instance, Coyne plays the bull. The issue of macromutations has a status with some evolutionary biologists akin to High Dogma, and they rush to attack any heresies in this direction. This process started as soon as evolutionary biology itself - Darwin was influenced by Lyell's revolution in geology that tiny incremental changes over eons could literally move mountains. In that era dramatic change was equated with creationism, or more broadly with missing the fundamental point that evolution could accumulate tiny changes and achieve big results.
More recently it has become clear that Lyell was wrong - specifically that a strictly incremental and slow version of geology is wrong. Dramatic catastrophes can play a role in landforms - often they play the dominant role.
Within biology the matter of macromutation continues to resurface repeatedly - as Coyne points out. Coyne clearly believes that the idea has no merit - which is fine, he is entitled to his opinion.
But he goes way overboard when he accuses Judson of being irresponsible. The fact is that very smart people do reexamine the idea periodically. It is ridiculous to suggest that Judson is "irresponsible" for airing this debate.
Indeed the very fact that Coyne goes on say that the idea comes up time and again, or that some of Judson's points are "common in the evo devo community" refutes the notion that it should be off limits. Regardless of whether you consider Judson a scientist or a journalist, there is nothing irresponsible here.
Coyne is a partisan of one side in an ongoing debate, and he doesn't like it that the other side has gotten some press.
Coyne may be right (or not, see below), but it is hardly irresponsible to suggest that he isn't.
Judson concludes by saying that there is only a "suggestion" that hopeful monsters have some valid basis. She is more than entitled to express her opinion without Coyne getting high and mighty.
That is mostly about his tone. However, I suspect that Coyne and his camp also wrong on the facts. Judson does not make the following points, but they are further suggestion that some aspects of macromutation MIGHT play a role in evolution. I will briefly list a couple.
There are two separate kinds of "macromutation" one can talk about. One is a large change in the genotype. The other is a large change in the phenotype. The two may or may not be correlated - one can imagine a huge dramatic shift in the geneome that has no corresponding change in the phenotype. Or a big change in the phenotype that was caused by a single base pair change. Each deserve to be considered as a macromutation of a sort.
On the genome side we know that individual genes are duplicated - that is clearly a huge change. The most dramatic form of this is whole geneome duplication, which we know has occured muliptle times in evolutionary history.
That can't have happened one base pair at a time - instead some copying error duplicated large stretches of the geneome, or all of it. That surely qualifies as a macromutation at the genomic level. There may (or may not) have been a correspondingly large change in the phenotype but that is a separate issue.
Other macromutations of the genotype include incorporation of foreign dna, for example via retroviruses and reverse transciptase. Many cases have been documented.
On the phenotype side we know that there have also been dramatic changes. Does anybody think that the incorporation of mitochondria to make eurcayotes happended one base pair at time? No, the current theory is wholesale adoption of a foreign organism, likely enabled by some genetic mutations in the host cell.
Work with knock-out animals, RNAI and gene splicing have shown that changing single genes, or even groups of genes, very dramatically can sometimes have no effect and sometimse have a big effect.
These cases are only suggestive - but that is the point here. I agree with Coyne that ultimately genomic research will figure this out. Until that research is done and the answer is in definitively it is worth discussing.
More generally the view of the micromutation crowd, ranging from Fisher to Coyne is that macromutations are unlikey to survive. This is the great and glaring unproven hypothesis - almost a religious point - with this camp
This is a quantitative issue, yet Coyne and others hand wave it away with no proof. They assert that "most" macromutations are harmful and could not survive (or could only in a greenhouse with human help).
How do they know?
The point here is one of competing rates - or probabilities - of very rare events.
First, we don't have any good way to measure the likelihood of survival of an animal with a macromutation (of either genotype or phenotype). Second, we don't know how often these macromutations occur. Without knowing those rates (which can depend on context and environment etc), how can Coyne be so dogmatic?
Even if the rate of survival is very low, nature is rolling the dice a lot of times. Even a miniscule probability of success will occur if you do sufficiently many trials. One in a billion tries is actually a high probability here - becuase nature has had way more than a billion trials. Indeed one can imagine situations where probabilities like one part in 10^20 or even lower could be important.
Fisher should have known this, but in his day they held incorrect views of the genome and its fragility to mutation. We know better now - small mutations can have big impact on the phenotype, and big mutations can have none.
Coyne accuses Judson of logical errors - his error is that he provides no proof for the assertion that macromutation must always have such a low probability of survival that it can't have played a role in evolution. It is a ridiculous position to take.
Ancedotal observation of a few sick bald chickens (an example he uses) do not count against this quantitative issue.
After getting a severe drubbing from geneticists, Eldredge and Gould retreated in 1993, claiming that they never suggested the idea of saltations.
Isn't Gould Mr. Hedge-his-bets-backtrack-and-say-everything? What I've read of him, he comes across as a person who, if discussing the question of whether or not black is white, would say "Black is completely different from white, but really they're the same and it's only a matter of difference in degree between, but in fact they're identical and they're also the same as 65,533 shades of grey in between, each of which are completely distinct from each other and black and white." I note others (e.g. Steven Pinker) have commented on this tendency of his.
An excellent blog. Insightful, intelligent and informed.
Get yourself a blog, now!
My only advice would be not to get caught up in every potential argument from those posting afterwards, as every single element of your article will find disagreement with someone.
From the above posts, it seems that Dr. Coyne's position has been misconstrued. I do not think that Dr. Coyne denies that genes of large effect can be important (see his American Naturalist paper with Orr, 1993). There are clearly examples of both genes of large effect and genes of small effect. But the question isn't whether these genes exist, but rather how often each type of gene contributes to species adaptations.
One comment cited melanism as an example of a trait controlled by a few genes of major effect. The key is that several genes have been implicated in melanism, not just one. Goldschmidt insisted that new lineages arose from major saltations caused by a single gene of large effect because he believed that gradual changes couldn't connect microevolution to macroevolution. But do we have evidence for just one mutation causing a new adaptation distinguishing two species?
This question can only really be addressed is with proper genetic data about adaptations within species and among species, which I'm willing to say we don't have enough of yet. (Enter Coyne's comment about needing to do genetics to discover genes for adaptations). The more we know about the genetic basis of traits, the better we'll be able to adjudicate the relative importance of gradualism and saltationism.
It would seem from Dr Coyne's opinion, that mutations with large effect, because of their alleged horrific pleiotropic effects, can only be admitted under the pampering conditions of domestication; hence the need to refresh our memories about the actual existence of genes with large effects in the wild.
Now, admittedly, I'm more of an embryo and fossil kind of guy. I am NO expert on the genetics of adaptation. Yet, it is unavoidable to notice statements like this from Orr Nature Reviews in Genetics 2005 (6: 119)
"Early empiricists, including Theodosius Dobzhansky, Hermann J. Muller, Kenneth Mather and Julian Huxley, claimed that there was considerable empirical support for micromutationism. For example,Huxley argued that selective advantages so small as to be undetectable in any one generation, are capable of producing all the observed phenomena of biological evolution.Evolutionary change is almost always gradual. Despite such confident statements, the case studies to which these early workers pointed were uniformly (and in retrospect, appallingly) weak"
I have become of course interested in what those case studies are, and what other cases have been proposed more recently. Maybe Dr Coyne is THE man to ask for these examples.
There are two recent papers that would challenge Coyne's dogma of the "primacy of gradual, stepwise evolution." Consider Eugene Koonin's paper in Biology Direct. ("The Biological Big Bang model for the major transitions in evolution" http://www.biology-direct.com/content/2/1/21) He writes that the principal "types" seem to appear rapidly and fully equipped with the signature features of the respective new level of biological organization. He goes on to propose a "Big Bang Biological model" for the major transitions in life's evolution.
In a paper by Gene Hunt in the Proceedings of the National Academy of Sciences, he reports on a study of the fossil record for statistical occurrences of three evolutionary models: directional change, random walk, and stasis. ("The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages" http://www.pnas.org/cgi/content/abstract/104/47/18404) Hunt examined evolving traits and reports the following:
"Evolution in these traits was rarely directional; in only 5% of fossil sequences was directional evolution the most strongly supported of the three modes of change. The remaining 95% of sequences were divided nearly equally between random walks and stasis."
The fossil record does not support gradualism. That concern goes all the way back to Darwin. The dogma of gradualism is so fiercely defended because any alternative would give comfort to creationists. But why not go to where the data leads? Isn't that the way science is supposed to work? The creationist model is a better fit of the empirical data than Darwinian gradualism. Science needs to acknowledge that and move on.
The appearance around 1870 of the cordgrass Spartina anglica -- I would personally consider this a macromutational change, but just out of curiosity, would or would people not classify this as a saltational leap, as it was essentially a one (or, arguably, two) step speciation event which happened extremely quickly?
Carl, thanks for airing this discussion. I would suggest that we've learned more about Prof. Coyne here than we have about evolution, development, genetics or even scientific history.
If he had merely addressed the weaknesses in Dr. Judson's piece, which are significant, then we'd have a valuable contribution from a heavyweight. Instead, he pulled out a grenade, and the mess he made is, in part, yours to clean up.
In his frenzied assault on unwarranted extrapolation, I wager he's done damage to experimental evolutionary biology of every kind, but I couldn't help but wonder whether he thinks that studies of Drosophila genetics can tell us anything about the evolution of anything other than Drosophila. His paragraph on the difficulty of understanding the past gave the impression that he would exercise care in addressing controversies in evolutionary biology. What followed was overwhelming evidence to the contrary.
What I found particularly disgusting was the cavalier dismissal of studies of domestication. (Paging Mr. Darwin. Mr. Darwin?) Exactly what is different about selection at the hands of humans, vs. selection influenced by, say, fruit flies? And I laughed out loud when he dismissed corn because it "would never thrive in nature because the seeds don't disperse." Wait, a plant that depends on an animal for reproduction?! Stop the presses! I wonder if there are any plants that depend on FRUIT FLIES for seed dispersal or pollination...
I'm sure that the debris from Coyne's grenade will soon be providing a feast for the anti-evolution vultures that dog his field. But that's not why his rant pissed me off. He's a brilliant scientist, and his Cassandra syndrome is understandable given the prominence of evo-devo ideas. His voice is too important to ignore, and that means he has to be more careful than this.
I am a bit worried that there seems to be very close similarities between Dr. Coyne's post one one of the commentators on Judson's blog. Specifically, comment 30 reads:
"Unfortunately, the hype about hopeful monsters is not deserved, because there are several errors in inference made in this piece. First, just because a mutation has a big effect WITHIN a species does not by any means imply that difference between species in the same trait are due to that mutation. There are mutations in humans causing dwarfism, for example, but its simply wrong to say that height differences between humans and chimps (or different populations of humans) are due to macromutations at the dwarfism gene. So much for the vulture example. Analogizing drastic mutations within species to differences between them is a common error, one reason being that large hopeful monster mutations often have bad side effects that make them less likely to evolve than mutations of smaller effect.
Second, the work on sex combs and Hox genes are ASSOCIATION studies, that is, the expression of a gene is associated with a difference in traits among species. But as all geneticists know, this does not mean that that very gene was instrumental, much less the only one, involved in producing species differences. The only way to show that is through direct genetic studies, involving either crossing or transgenics. In most species this cannot be done.
Its telling that the foremost exponent of evo-devo, Sean Carroll, does not subscribe to the macromutation theory, and he is the author of one of the studies cited by Judson.
As an evolutionary biologist, I am distressed that work in our field is both simplified and somewhat misrepresented to make a point. Until we have more genetic studies, we simply cant assess the role of macromutations in evolution. There are still no cases in which a major difference between groups is known to be based on changes in a single gene.
Posted by Ronald Fisher"
That seems a bit close for comfort.
No, but it is overwhelmingly likely that it happened by smaller steps from facultative to obligate endosymbiosis, including loss of mitochondrial genes or their transfer to the nucleus in smaller chunks. Unless you have some reason to assume that it was nothing like the endosymbionts where we can observe "evolution in action" today.
The devidence for exogenetics, and the implication that some Lamarkian adaptation could occur, raise the possibility that genomes might have a battery of dormantadaptations that could be switched on by environmental effects, including potential size changes.
Great blog BTW!
Considerable impediment to progress on this topic is nothing but cultural artifacts. Consider Dr Coyne: he falsely equates punctuated equilibria and saltationism. But THEN on the other side, we unfortunately have too many that see saltationism as fitting their particular revolutionary new picture, usually full of fantastic mechanisms and extraordinary happenstances and a little dose of, well...crackpottery; For instance, analogies to the big bang of cosmology impress as worthless (despite the catchy title).
Another error is that some say classical darwinian selection rules for evolution within smaller clades (microevolution, for instance), but that saltationism is needed to explain the differences between higher taxonomic orders. This is not true, you are simply more different if you share a more remote common ancestor. Prud'Homme et al 2006 (PNAS) find developmental mechanisms affect both macro and microevolution in basically the same way: Both reveal "regulatory regions" that constrain evolution. "Saltation" was as important when big clades diverged eons ago (when they were the newest "branchtips") as it is nowadays in ongoing processes of evolution and speciation.
I should have said "epigenetics" not "exo..." sorry!
http://en.wikipedia.org/wiki/Epigenetics
After seeing Olivia Judson's Jan. 22nd piece on macromutation on the New York Times website, I thought of putting a comment on the website, but decided against it- there are more pressing battles to be fought in explicating evolutionary biology to the public, and the Times didn't actually publish the piece (merely posting it). I was thus greatly pleased to read Jerry Coyne's guest post here a few days later. He put the 'hopeful monster' debate in its historical context, and rebutted. Judson's arguments. I was somewhat taken aback by some of the ensuing comments posted here, which exhibit an almost breathtaking range of misunderstandings. While taking to heart the advice of The Monkey Man, who advised Coyne not to try to answer every criticism, I feel compelled to take up the cudgels.
I should perhaps begin by noting that, although Coyne and I shared, at different times, the same graduate adviser, Coyne was and is a geneticist, while I was and am a herpetologist. Thus my views, and the overlap between them and Coyne's, do not stem from some shared disciplinary chauvinism, or over-commitment to the centrality of genetics. (I don't think Coyne's do either, as some commenters seem to suggest, but it's harder to make the case that a non-geneticist is too much devoted to genetics.)
Coyne makes two of the chief (and traditional) criticisms of hopeful monsters: mutations of large effect are usually accompanied by deleterious pleiotropic effects, which would make such mutations selected against; and the existence of a simple genetic basis for a trait does not mean that the evolution of the trait was correspondingly simple. The first point is universally acknowledged, at least at some level, which is why even proponents of hopeful monsters suppose their occurrence to be rare. As regards the latter, let me give an example not used by Coyne. One of the earlier-known homeotic mutants in Drosophila converts the halteres into wings. But this does not mean that halteres (or wings!) arose via a single mutation; rather, the gene switches on (or off, depending on your point of view) parts or all of a developmental process. The origin of the trait is the origin of the developmental process, not the switch. To give another example, Sewall Wright studied a condition in guinea pigs called otocephaly which, in its most extreme form, results in the affected guinea pig lacking eyes. The condition has a relatively simple (but not single gene) genetic basis. But the mammalian eye did not evolve in one or two steps on this genetic basis, and there is a long series of eyes with varying features in extant chordates (as well as some relatively recently found and tantalizing fossils) which provide a firmer basis for inferring the history of eyes. That current mutational effect does NOT equal evolutionary origin is by now so well known, that to argue that it does is a fallacy worthy of its own name- and Coyne calls it the 'macromutationist fallacy'.
There are at least two other traditional criticisms of macromutation that Coyne does not fully address. The first is that evolution is a populational process- in diploid sexual species, individuals with mutations must find mates with whom to pass their new traits on to the next generation. While a macromutation does not necessarily debar an individual from finding, attracting, and successfully mating with another individual, it might make it more difficult, and the greater the phenotypic effect of the mutation, the greater the difficulty. Thus hopeful monsters need to be worried not just about surviving the deleterious effects, they also have to worry about finding a mate. (In plants with vegetative reproduction, polypoidy, which seems the closest thing genetically to Goldschmidt's systemic mutations, does occur much more commonly than it does in animals.)
The second concerns the relationship between the organism and its environment. Macromutationism supposes that structure precedes function- an individual finds it has some drastically restructured body, and it must find a place it can live. The famous herpetologist G.K. Noble was a mutationist, and supposed that the expanded toe tips of tree frogs arose mutationally, and that the frogs then had to find their way into the trees. This is the flip side of naive versions of adaptationism- the environment poses problems, which the organism must solve by evolving adaptations. Under macromutationism, an organism finds it has a solution, and then must look around for an environment that poses the problem it just happens to have the solution to.
Let's take the evolution of whales as a not entirely arbitrary example. Under naive adaptationism, some early artiodactyls are pitched out to sea, and must evolve flippers, tail flukes, etc. to solve the hydrodynamic problems of locomotion. Under macromutationism, some poor, hopeful artiodactyl is born on land with flippers, tail flukes, etc., and must find its way to water (and also hope there's another hopeful artiodactyl out there to mate with). But neither of these views seems right. The organism's environment is not purely imposed by external circumstances, but arises as a complex interaction between the organism's structures and behaviors, and environmental characteristics (R.C. Lewontin likes to say, perhaps overstating a bit, that organisms create their environments). Structure and function are intertwined.
For whales, we in fact know from fossil evidence that they evolved through a long series of intermediate morphologies and ecologies, and not via a hopeful monster. There are, indeed, in mammals, teratological flipper-like limbs that occur in normally-legged species. But that's not how whales got flippers. Nor, probably, did seals, manatees, etc., although the fossil record is not so compelling for these groups. The living sea otter provides us with an example of a step in the origin of flippers from feet, and shows the corresponding function/ecology.
Perhaps the best argument against hopeful monsters is that we have, at least in vertebrates, many fossil sequences documenting the origin of higher taxa via numerous intermediate steps. We have long known that tetrapods evolved from lobe-finned fishes. The discovery of fossils near the transition such as Panderichthys ,and the very recent discovery by Neil Shubin, Ted Daeschler and Farish Jenkins of Tiktaalik, is filling in the structural differences between fish and amphibian, so that we can see exactly how legs gradually arose from fins. The fossil record is a far cry from Richard Goldschmidt's notion that simple changes in thyroid hormone levels might turn a fin into a foot in a single step. Another excellent example is the transition between reptiles and mammals. As long ago as the 19th century the herpetologist E.D. Cope identified early synapsids as the closest relatives of mammals. At the time, it could be asked (and is asked to this day by creationists who either don't know or deliberately ignore the fossil record), "how could reptilian jaw bones become mammalian ear bones?" A macromutation (or a miracle) might have seemed a plausible answer, but in fact we now know, thanks to the work of Fuzz Crompton, Farish Jenkins, and many others, more or less exactly how this occurred- by many steps, over millions of years.
Metameric (segmentally repeated) structures allow production of whole new segments without great alteration of the developmental machinery, and this might allow changes that could perhaps be described as macromutational (although arguably not; and variation in plate number in sticklebacks, although extremely interesting, would be rather small consolation to Goldschmidt). In vertebrates, though, although vertebral number has varied considerably (along with the corresponding segmented muscles, nerves, blood vessels, etc.), limb number, despite occasional teratological variation, has never varied from four, except for losses of limbs, which in all well known cases have been by gradual reduction (e.g. lizards, whales).
The take home lesson of vertebrate paleontology and comparative morphology is that much of evolution is the gradual adaptive modification of pre-existing structures and their underlying developmental programs.
One specific example of Judson's that Coyne addressed from a genetic point of view that I would like to address form a comparative morphological point of view is cephalic baldness in chickens and vultures. Judson supposes the first indicates how the latter arose, but admits to not knowing for sure. My first thought, as someone who has actually measured birds's heads (I've dabbled in ornithology), is that exactly how much feathering there is on a bird's head varies considerably within and among species. A few minutes reflection and checking some pictures confirmed that there is a wide range of nakedness of the head. Caracaras lack feathers around the eyes and cheeks, picathartes are bald to about the middle of their heads, guinea fowl are mostly naked but have lines of feathers running up the neck and head, and vultures are bald on head and neck. A real ornithologist could probably provide more examples. Now the examples I give do not form a phylogenetic series, but like many of Darwin's arguments, they provide a "how possibly" argument for how baldness can arise gradually. As for Darwin, such arguments are an effective response to the "argument from personally incredulity" (which is not what Judson used; but it does exclude accepting macromutation in default of any alternative). Thus study of comparative feathering does not cry out for a macromutational origin of baldness.
Disregarding briefly The Monkey Man's sage advice, let me briefly address two specific criticisms of Coyne. One is that Coyne is following a discredited Lyellian view of geology. If Coyne mentioned geology, I missed it. I will mention though that our modern theory of the earth, plate tectonics, would have made Charles Lyell quite happy, because it provides not only for uniformity of process, but uniformity of state- the cycling of continental agglomeration and splitting over hundreds of millions (if not billions) of years would fit nicely in his view of the earth in dynamic equilibrium. This uniformity of state is something which, as Lyell finally admitted, eluded him for the condition of life on earth. The other is that Coyne disregards Darwin's lessons on the importance of the study of variation under domestication. Quite the contrary, Coyne's points are precisely Darwinian. Darwin used artificial selection and variation under domestication as vera causae for the power of cumulative selection of variations; Darwin did not think the particular variations under domestication especially germane. Indeed, the reason Darwin, unlike Wallace, used arguments about domesticated forms is because Darwin saw that the domesticated breeds would usually be at a disadvantage in nature, and that selection would quickly revert them to "wild type". Wallace saw this reversion as indicating changes under domestication were unstable, rather than the result of changed selection pressures as Darwin did.
Finally, I note that creationists are already here in the comments touting macromutation as showing creationism is correct. This has more to do with the ignorance of creationists than anything Coyne's critics have said. The ability of creationists to misconstrue the views of evolutionists is legendary- P.Z. Myers has noted a debate with a creationist in which the creationist insisted S.J. Gould didn't believe in evolution, but rather punctuated equilibrium!
I am not sure if Gregory Meyer's posting (#30) includes my above post (#15) as conveying a "breathtaking range of misunderstandings", but I will try to make clearer. Everyone, including Meyer, is crossing the wires. "Hopeful monsters" is indeed Richard Goldschmidt's, but there are two main idea sets on "macromutation," that due to de Vries and that due to Goldschmidt. The de Vries macromutation is primarily phenotypic - one sees immediately that something "macro" has happened at the organism level. Goldschmidt's (at least that set out in his 1940 book that Olivia Judson cites) is primarily genotypic. It is a change in the genome that may build up progressively over many generations until the organism suddenly flips and startling new phenotypes can then, and only then, gain a foothold.
Goldschmidt called this a change in "reaction pattern."
Anthropologist Gregory Bateson (1904-1980) later saw this in terms of a change in genome context. So there can be the conventional mutations that can change individual genes (and be manifest as such), and other mutations that can build up (without external manifestation) until they cumulatively change the "reaction pattern" of a chromosome or set of chromosomes. To distinguish the latter from individual micromutations Goldschmidt called them macromutations. Until manifest in a change in phenotype, these macromutations are invisible.
So people are mixing up Goldschmidt and de Vries. Goldschmidt's ideas have roots in ideas William Bateson (Gregory's dad) was enunciating in the early decades of the 20th century. People tend wrongly to conflate William Bateson and de Vries, and hence create even more problems. More on this may be found in our new biography of William Bateson, due to be released by Springer (New York) in April (see: http://post.queensu.ca/~forsdyke/book04.htm)
I think it's safe to say that Gould sometimes presents a moving target.