Why exaptation is an unnecessary term in the science of form

December 28, 2015 • 2:30 pm

by Greg Mayer

The most important finding of vertebrate comparative morphology and paleontology is that most of evolution is the gradual, adaptive, modification of pre-existing structures (or, better, pre-existing developmental programs, which result in the structures).  The point about pre-existing structures is very important– the history of evolution is to a great extent the history of making due with what you have– “tinkering”, as François Jacob called it. The current phenotype is where you start, and there is a range of mutationally accessible phenotypes that is determined by the developmental system, the environment, and the genotype. This mutationally accessible region will only rarely include completely new structures.

As mammals, WEIT readers may have wondered why it is so difficult for them to get food to come out of their noses while eating (it usually requires vigorous coughing, laughing, or sneezing), while their pet aquatic turtles can do so effortlessly, small food particles floating gracefully out of their nostrils while they eat. The reason is that mammals have a secondary palate– reach in and tap the roof of your mouth– that’s it, right there. It is a shelf of bone that separates the air passage, which goes from the nostrils to the glottis, from the food passage, which goes from the mouth to the esophagus. In (most) turtles, there is no secondary palate, so the air and food passages are one passage, thus allowing food to exit the nostrils. Where did the secondary palate come from? It is not a new bone(s), but a series of medial processes, off the very same bones found in turtles, that meet in the midline to form a complete shelf. Turtles, having a low basal metabolism, do not need to breathe incessantly, while mammals, with their high metabolism, must generally be breathing and eating all the time– the separated passageways allow mammals to breathe while chewing. The gradual modification of these bones to form a secondary palate (and, somewhat less clearly, the crucially associated soft palate) can be traced in the fossil record. The drawback to the way mammals eat is that when finally you have to swallow the food, the lungs are ventral to (i.e. below) the digestive tract, even though your nostrils are dorsal to (i.e. above) your mouth, and the air and food streams must cross. So, if you sneeze/cough/laugh real hard just as your food is crossing over the air passage, it can be blown into the air passage, and come out your nose.

Mammalian swallowing and breathing is thus based on the same bones, digestive tract, and lungs, arranged in the same basic way, as are found in turtles, and in our common reptilian ancestor. In mammals, the pre-existing structures have been “tinkered” with, in a series of documented steps, to arrive at the current state, which allows for a lot of eating and breathing, which in turn allows for a high metabolic rate (and hence being warm-blooded), although since the lungs remain below the gut, you can choke on your food. (Had engineers designed vertebrates, they never would have crossed the air and food passages.)

What brings all this to mind is Jerry’s mention yesterday of Steve Gould’s concept of “exaptations”, noting that the 7th day of evolution video stated that penguin wings are an”exaptation”, because “not every trait is an adaptation, and they don’t all have a point.” This is surely one of the most unproductive, and, indeed, wrong, ways to look at penguin wings. Penguin wings are in fact adaptively modified pre-existing structures; the earliest known penguins in the fossil record, were flightless swimmers, but not as modified for this as later penguins. The notion that a change in function (flying to swimming, in this case) necessitates a new terminology was argued, quite unsuccessfully, by Gould and Elizabeth Vrba in 1982.

Composite skeleton of Waimanu tuatahi from Slack et al. (2006), via March of the Penguins.
Composite skeleton of Waimanu tuatahi of the Paleocene, one of the earliest penguins, from Slack et al. (2006), via March of the Fossil Penguins.

“Exaptation” is an unnecessary term in the science of form. It confuses more than it clarifies. It ignores the historical component of adaptive evolution (which is curious for Gould, since he frequently, and often correctly, argued for the importance of historical considerations; his animus against natural selection must have overcome his historical instincts in this case).  The great paleontologist George Gaylord Simpson attempted to rehabilitate the term “preadaptation” to cover the not uncommon situation where a pre-existing structure undergoes a change of function; once there is a new function, then “postadaptation” will refine the structure to fit the new function. The morphologist Carl Gans suggested that what he called “excessive construction”– the ability of a feature to perform at least tolerably in circumstances other than the usual ones– could often form the basis for preadaptation. (Gans substituted “protoadaptation” for “preadaptation”, finding the latter term too freighted with unfortunate associations with mutationism, of which Simpson sought to cleanse it, to be used.)

I find preadaptation, shorn of its mutationist connotations, a perfectly serviceable concept. Thus, wings on aquatic birds are a preadaptation for swimming in the water. Behavioral flexibility allows the wings to be used in a new way, which then induces a new selective environment, and postadaptations will then further suit the structure to these new conditions of existence. But even more productive, I think, is the notion of “sequential adaptation”, based on Richard Swann Lull’s notions of primary and secondary adaptations (and related to W.K. Gregory’s related concepts of caenotelic vs. paleotelic and habitus vs. heritage), which provides a much better way of looking at changes of function. (I’ve long attributed the phrase “sequential adaptation” itself to Lull, but after a rereading I can’t find that he used it; it was my term for summarizing his views. Lull, by the way, was Simpson’s doctoral adviser.)

So how do we look at the wings of penguins under this view? Certain dinosaurs’ front legs (they already had front legs, of course– they were preexisting structures) became adapted for flight– that is, there were modifications in the structures that conferred higher fitness on their possessors by virtue of the presence of the modifications.  Are the wings of birds an “exaptation”? No. Wings, qua wings, are an adaptation for flying. The wings of certain birds became adapted for swimming– the “flippers” of penguins. The bones have become solid, more robust, dorsoventrally compressed and knife edged, all of which improve their function for diving (not all of these were fully present in the earliest known fossil penguins). Each of these modifications is an adaptation. In Lull’s terms, the wing is a primary adaptation (for flight), the flipper a secondary adaptation (for swimming). But the wing itself was a secondary adaptation of the primary adaptation of the locomotory forelimb of dinosaurs– and so on back in time. They are a series of sequential adaptations. The error of “exaptation” is to think of traits or features of organisms as unanalysed wholes without a history: penguin flippers are are not merely “flippers”, but a whole suite of features, including many bones, muscles, and behaviors for their use. And the flippers have a preceding history as wings, front legs, and so on ad not-quite-infinitum. If “exaptation” means that later adaptations are based on the pre-existing structures, then the term is vacuous– all adaptations are then exaptations.

A case noted by Simpson as preadaptation involves the predatory behavior of keas (Nestor notabilis), the large alpine parrot of New Zealand. Keas eat sheep (or at least parts of them, since the sheep may survive), by cutting through the skin with their sharp hooked beaks.

Keas are naturally omnivorous, so what we have is an expansion of the dietary range, enabled by the pre-existence of a wicked beak. The beak is an adaptation to wide ranging foraging on and in the ground, and on and in the vegetation (excavating logs and such).  If there arises an innate (as opposed to learned) aspect of sheep feeding, or the bill itself experiences selection for features that enhance the ability to feed on the sheep, there would would then be secondary, or sequential, adaptations. At this point, though, feeding on sheep may well be behavioral flexibility with the available tools (Gans’ “excessive construction”, providing the basis for “protoadaptation”).

We not only don’t need the term “exaptation”, it actually hinders understanding, by suggesting that non-adaptive processes are at work (which was Gould and Vrba’s explicit intention), when in fact we have a series of sequential adaptations.

[And I must give here a strong recommendation to the website March of the Fossil Penguins by Daniel Ksepka, which I discovered while writing this post.]

Gans, C.  1979.  Momentarily excessive construction as the basis for protoadaptation.  Evolution 33:227-233.

Gould, S.J. and E.S. Vrba. 1982. Exaptation- a missing term in the science of form. Paleobiology 8:4-15. pdf

Jacob, F. 1982. The Possible and the Actual. Pantheon Books, New York.

Kirsch J.A.W. and G.C. Mayer. 1998. The platypus is not a rodent: DNA hybridization, amniote phylogeny and the palimpsest theory. Philosophical Transactions of the Royal Society B 353:1221-1237.  pdf

Lull, R.S. 1917. Organic Evolution. Macmillan, New York.  Internet Archive

Simpson, G.G. 1953. The Major Features of Evolution. Columbia University Press, New York.

Slack, K.E., C.M. Jones, T. Ando, G.L. Harrison, R.E. Fordyce, U. Arnason, and D. Penny. 2006. Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution. Molecular Biology and Evolution 23:1144-1155.