Hopeless Monsters–A Guest Post from Dr. Jerry Coyne

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.