Why wither Goldschmidt?

On November 23rd, 1858, T.H. Huxley wrote one of the most famous letters in the history of science to Charles Darwin. While the letter is perhaps most widely known for Huxley's staunch support of On the Origin of Species by Natural Selection against the opposition both were sure would come out against the book (Huxley opining that "I am sharpening up my claws & beak in readiness."), the letter also contains another important quote. As much as Huxley was taken with Darwin's book, he did have some reservations about one aspect of Darwin's idea that came up over and over again;

The only objections that have occurred to me are 1st that you have loaded yourself with an unnecessary difficulty in adopting 'Natura non facit saltum' so unreservedly. I believe she does make small jumps--and 2nd. it is not clear to me why if external physical conditions are of so little moment as you suppose variation should occur at all--

Huxley ultimately voiced the same criticism about "jumps" again in a review of Darwin's book published in 1860, writing;

A frequent and a just objection to the Lamarckian hypothesis of the transmutation of species is based upon the absence of transitional forms between many species. But against the Darwinian hypothesis this argument has no force. Indeed, one of the most valuable and suggestive parts of Mr. Darwin's work is that in which he proves, that the frequent absence of transitions is a necessary consequence of his doctrine, and that the stock whence two or more species have sprung, need in no respect be intermediate between these species. If any two species have arisen from a common stock in the same way as the carrier and the pouter, say, have arisen from the rock-pigeon, then the common stock of these two species need be no more intermediate between the two than the rock-pigeon is between the carrier and pouter. Clearly appreciate the force of this analogy, and all the arguments against the origin of species by selection, based on the absence of transitional forms, fall to the ground. And Mr. Darwin's position might, we think, have been even stronger than it is if he had not embarrassed himself with the aphorism, "Natura non facit saltum," which turns up so often in his pages. We believe, as we have said above, that Nature does make jumps now and then, and a recognition of the fact is of no small importance in disposing of many minor objections to the doctrine of transmutation.

Nearly 150 years after Huxley wrote about what he felt was an unnecessary strictness of Darwin's theory of evolution by natural selection, the concept of whether nature makes "jumps" (or saltations, if you prefer) is still controversial. It is not Darwin or Huxley that are often cited in the modern debate, however. The current lightning rod for the argument surrounding saltation is the late geneticist Richard Goldschmidt, who famously coined the phrase "hopeful monster" to try to explain that large-scale evolutionary changes cannot be understood by within-species changes writ large and developed his own alternate view of evolutionary change. Most recently, appropriately right on the heels of my post about uniformitarianism vs. catastrophism, University of Chicago scientist Jerry Coyne has responded via the blogosphere to a piece called "The Monster is Back, and It's Hopeful" by Olivia Judson on a New York Times blog, and it seems that neither Judson nor Coyne have gotten things entirely right when the question is "Is there hope for this 'monster'?"

There are several problems with the hopeful monster concept in evolutionary biology, primarily that the phrase has appeal but is so vague (and hence widely used) that it is difficult to ascribe a true meaning to it. Admittedly I have not read any of Goldschmidt's work, The Material Basis of Evolution perhaps being the most important to understanding his position, but after a quick search of the literature it seems that the term "hopeful monster" is widely, if inconsistently, used. The general meaning of the phrase would be an organism that had undergone a major evolutionary change (a saltation) in one generation, the organism possessing whatever biological innovations that may have arisen spurring the branching of new evolutionary groups. Such changes, Goldschmidt argued, may have occurred during development, especially since small changes early on could have larger consequences as the organism grew and developed. In this context, hopeful monsters would have the most influence on the history of animal life on earth around the time of the Cambrian explosion (and the preceding Ediacaran explosion, as inferred by Shen, et al.), changes in body plan having much greater effects later hypothetical "monsters" like a bird losing feathers over part of its body (as in Judson's article). Saltational changes in existing derived vertebrates could, hypothetically, open new evolutionary pathways, but it seems that the greatest potential for influence is much further down the evolutionary bush.

Despite what influences saltations could have had (if ever confirmed to be real), the hopeful monster concept ultimately suffers from issues that have dogged other controversial topics in geology & biology. When considering the "tempo and mode" of evolution (to borrow part of the title of G.G. Simpson's influential work that preceded Gould & Eldredge's punctuated equilibria), how fast is fast? We can still call evolution gradual (in that there are understandable gradations between one generation and the next through time that allow us to detect the relatedness of species) while rejecting a uniformity of rate. (Indeed, the idea that the rate of evolution is variable is hardly controversial, although the reasons for the quick change and stasis are still hotly debated.) Likewise, in terms of the hopeful monster model, how "big" does a mutation have to be for it to be considered a macromutation? Are we speaking of the size of the change, the size of the effect, or something else entirely? What sort of pattern should we expect if such a change were to take place? For the hopeful monster model to make sense the mutation would have to be beneficial and not reproductively isolate the organism that possessed it (it would have to leave viable offspring that could reproduce themselves, this problem being a major barrier for sexually reproductive species, especially derived ones) and open up some new evolutionary pathway for the lineage that could be detected. Indeed, the pathways that a saltation would open up are just as important as the beneficial mutation itself; if a saltation occurs but doesn't "go anywhere," ultimately being extinguished while the rest of the ancestral population continues on, does it really fit the concept?

This is the main problem with Judson's proposal that vultures are a good example of a hopeful monster. Vultures lack feathers around their heads, Judson's piece suggesting that this is an adaptation to prevent fouling whatever feathers would normally be present when feeding on a rotting carcass. As Judson suggests, this change may have occurred in a jump (or perhaps a series of smaller jumps?) rather than a feather-by-feather reduction until everything was "just right." The fact that other groups of birds like storks also are truly bald would seem to support this view, but even if avian baldness is the result of saltation I don't think it was what Goldschmidt had in mind. What new niches or pathways were opened up? The change would have allowed birds that would have (presumably) already been scavenging to do so more effectively; the ancestors of vultures weren't doing something else for a living, became bald, and suddenly realized their problems had been solved. In his response to the claims made by Judson, Jerry Coyne provides explanations as to why the vulture example picked on the NYT blog falls flat (although he makes his own mistake about naked-necked chickens), although the tone of the piece was a little harsh. Despite Coyne's insistance that saltations simply do not now and have not ever existed, though, I think the question of whether saltations occur or not is still largely up in the air; firm evidence still appears to be lacking, but I think it is a useful question to ask (even if only to confirm that no such event occurred).

The hopeful monster hypothesis seems to play a part in the larger issue of a changing Modern Synthesis of evolution (or synthetic evolution), the central ideas of the synthesis being described by Ernst Mayr this way;

The proponents of the synthetic theory maintain that all evolution is due to the accumulation of small genetic changes, guided by natural selection, and that transspecific evolution is nothing but an extrapolation and magnification of the events that take place within populations and species.

While I would disagree with the statement of Gould's 1980 paper that the Modern Synthesis, as stated above, is essentially dead, I would say that the definition provided by Mayr is far too narrow, and every once in a while a new article pops up about the emergence of a new synthesis. It's my impression that the state of evolutionary science has been changing for quite some time (see Kutschera & Niklas, 2004) even if we have not reached a point where we can say a new synthesis has been created, yet there are plenty of straw man arguments and mischaracterizations to go around. (Perhaps future historians of science will be able to pick a time when major shifts were being made, but being in the thick of things it's awfully hard to tell at the moment.) As I hinted in the introduction of this post, the whole issue reminds me a bit of the classic uniformitarian vs. catastrophist debate in geology, and while it is far too early to say that there is a "winning" side (nor would I want to side with some scientists over others merely because they stood under what I felt was the proper banner) it seems that there is presently a debate going on in evolutionary science over the presence of "biological catastrophes," unique and rare events that could send a lineage branching off in a new direction.

Another problem with the hopeful monster idea is that it has focused far-too-narrowly on derived vertebrates for examples (although Goldschmidt himself did most of his work on gypsy moths). While I will be the first to admit that my the zoological objects of my interest are often toothy, fierce, and have a backbone, such representatives of life on earth only make up a tiny fraction of the historical whole. If anything (as hinted by Hintz, et al.), plants and members of other kingdoms may yet provide the best evidence for saltational changes. Even if saltations are discovered, though, they may not be understood as such, and a major problem for proponents of hopeful monsters may end up being a matter of definition, especially given the ability for Goldschmidt's phrase to polarize. So far, though, most fields have turned up little evidence of saltation, but the study of development and the emerging field of epigenetics may yet provide confirmation or refutation of the concept of "natura non facit saltum," especially since even a rare event in the history of life on earth could still be very significant. In terms of the present conversation though, as much as I might be loathe to have such a wonderful phrase wrested from me, perhaps it would be best to leave hopeful monsters lie. The phrase carries with it so much baggage that its primary effect seems to be making up minds before data can be shared. Perhaps, if a true saltation is ever identified, a more rigorous definition might be able to be formulated, but for the moment it is probably a concept best invoked with great care. Still, while I might not be as sure as Huxley that nature makes leaps, it is important to keep asking the question, and I see no reason to close the coffin on the general concept of saltation yet.

The hopeful monster concept, as it exists today, is more-often-than-not a watered down version of what Goldschmidt had originally proposed (a concept that has unfortunately overshadowed nearly everything else he ever did). Certainly he should be duly credited for the concepts he proposed, but the present arguments about large-scale evolutionary changes in one generation are only loosely connected to Goldschmidt's alternate evolutionary vision. Indeed, Goldschmidt's ideas about genetics were generally unsound and he viewed species as far more disparate than they actually were, (therefore the gap that Goldschmidt inferred between microevolution and macroevolution was not so drastic as he proposed). For these reasons he seems to be more important in the history of biology than the way in which biology is presently studied, at least in the context of his later hypotheses (as Dietrich notes, he did make some important contributions earlier in his career). The best way to close this post chock-full of armchair speculation, then, may be to quote the words of Richard G. Harrison when The Material Basis of Evolution was republished in 1982;

It is appropriate that all evolutionary biologists read Goldschmidt's work so that they can know first hand what he did and what he said. Goldschmidt has been much criticized and, more recently, much praised. I cannot agree with Gould's statement in the Introduction that Goldschmidt should "be weighted equally with his self-proclaimed Darwinian opponents." I do believe that many issues that the neo-Darwinians thought resolved still remain open and that Goldschmidt should be credited for his imaginative thinking and for his clear emphasis on development-on gene expression rather than on gene transmission. But with regard to understanding the genetic basis of phenotypic change and the origin of new species, we should free ourselves of constraints imposed by past debate and turn for our ideas to modern developmental biology and molecular genetics. Evolutionary biologists seem particularly fond of reviving old themes and renovating them to serve as foundations for the elaboration of new theories. In many cases (and the current controversy about macroevolution and speciation is certainly one such case) we would do much better to start afresh.

Further reading on the blogosphere;

"'Hopeful Monsters': Nothing in Evolution Makes Sense Except in the Light of E. coli (and Shigella)" at Mike the Mad Biologist

"Hopeless Monster? Not so fast!" at A Blog Around the Clock

"Macromutations and Punctuated Equilibria" at The Sandwalk

"Nature makes no leaps..." at Evolving Thoughts (definitely check this one out!)

"Hopeful Monsters and Hopeful Models" at Greg Laden's Blog

"Jerry Coyne smacks down Olivia Judson" at Gene Expression

"Coyne is on the Loom" at Pharyngula

References;

Charlesworth, B. (1982) "Hopeful Monsters Cannot Fly." Paleobiology, Vol. 8 (4), pp. 469-474.

Dietrich, M.R. (2003) "Richard Goldschmidt: hopeful monsters and other 'heresies.'" Nature Reviews: Genetics, Vol. 4, pp. 68-74

Gould, S.J. (1980) "Is a New and General Theory of Evolution Emerging?" Paleobiology, Vol. 6 (1), pp. 119-130.

Harrison, R.G. (1982) "Return of the Hopeful Monster?" Paleobiology, Vol. 8 (4), pp. 459-463.

Hintz, M.; Bartholmes, C.; Nutt, P.; Ziermann, J.; Hameister, S.; Neuffer, B.; and Theissen, G. (2006) "Catching a 'hopeful monster': shepherd's purse (Capsella bursa-pastoris) as a model system to study the evolution of flower development." Journal of Experimental Botany, Vol. 57 (13), pp. 3531-3542

Kutschera, U.; Niklas, K.J. (2004) "The modern theory of biological evolution: an expanded synthesis." Naturwissenschaften, Vol. 91 (6), pp. 255-276