This Week's Citation Classic

The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. S. J. Gould, R. C. Lewontin Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 205, No. 1161, The Evolution of Adaptation by Natural Selection (Sep. 21, 1979), pp. 581-598.

I confess I am not a huge fan of Stephen Jay Gould. Although his extensive science writing is often charming, and has helped popularize evolutionary biology across a much broader spectrum (Wonderful Life was wonderful!), I consider much of his evolutionary thought simply wrong headed and strange. I won't go into specifics here, *cough, cough, punctuated equilibrium*, but some of his work is basically window dressing. I haven't read his latest opus, The Structure of Evolutionary Theory (its size, 5.1 pounds, is quite daunting; I'm waiting for the Reader's Digest version) so I could be wrong here, but I doubt it.

Dick Lewontin, on the other hand, is a great evolutionary biologist and has made many seminal contributions to the field.

Despite my misgivings about Gould, I found the paper on the Adaptationist Programme to be spot on. First off, it has a fantastic title. Not a cutesy punning title, but a novel, eye-catching title with side references and metaphors that actually make sense.

Second, the paper addressed a real concern in evolutionary biology. Despite G.C. Williams tour-de-force, Adapatation and Natural Selection, the study of adaptation in the '70s still suffered from wishy-washy, uncritical thinking (Larry Moran might argue still does today!). The problem was Just So stories (so named after the Kipling kiddie stories about How the Leopard Got His Spots etc.) where anyone can invent reasons, however fanciful, for why certain phenotypic traits exist.

Gould and Lewontin cite experimental work by D.P. Barash as an example of this problem.

Barash mounted a stuffed male near the nests of two pairs of bluebirds while the male was out foraging. He did this at the same nests on three occasions at ten-day intervals: the first before eggs were laid, the last two afterwards. He then counted aggressive approaches of the returning male toward the model and the female. At time one, aggression was high toward the model and lower toward females, but substantial in both nests. Aggression toward the model declined steadily for times two and three and plummeted to near zero toward females. Barash reasoned that this made evolutionary sense, since males would be more sensitive to intruders before eggs were laid than afterward (when they can have some confidence that their genes are inside). Having devised this plausible story, he considered his work as completed.

The explanation misses an obvious alternative. Perhaps the males approached the models a few times, learned that they were fake, and thereafter no longer responded to them. The proper way to conduct this experiment is to expose a male to the model once... either before or after the eggs are laid. The experiment was replicated by Morton et al. (1978) who found no evidence for anti-cuckoldry behavior.

Gould and Lewontin believed that too many biologists were simply making up similar stories for every conceivable trait. Perhaps some organismal traits have no function! Take the belly button. Maybe it evolved to collect lint so that cavemen would have a source of fiber for their diets! Uhhm... not likely. The belly button is an example what Gould and Lewontin would call a spandrel. The San Marco spandrels are so beautifully decorated with mosaics that one could be convinced that they were designed expressly to display mosaics. Not so! Spandrels simply hold up the ceiling; they were painted to make them look pretty. Belly buttons serve no function; they are simply the remnant of the umbilical connection between the mother and fetus.

So how should one determine whether a certain trait is an adaptation? A good adaptive hypothesis will make predictions concerning the trait it seeks to explain. Also several criteria should be met: (1) trait variation must affect fitness or a component of fitness; (2) the hypothesis of adaptive variation must be confirmed by either manipulating the selective environment or the phenotypic trait itself; and (3) the mechanistic link between the trait and fitness must be demonstrated.