Copyright (©) Kellar Autumn 1995
Do not use or copy without permission of the author
Many introductory evolution courses would introduce adaptation by putting a couple of equations on the board or showing some slides with amazing features of animals uniquely adapted to extreme environments. The word adaptation, like fitness, has such a common usage and a long history that one would think there is little to argue about in its definition. Nothing could be farther from the truth! Debate over the meaning of adaptation predates Darwin and has generated dozens of articles in major publications in just the last few years. What is the problem and why are we still arguing about it?
In brief, the problem is: what explains diversity: Structure or Function?
I will present a brief history of the adaptation controversy and show that it represents a fundamental split in the way biologists approach their work today. I should mention that I think we are closer now to a consensus on this issue than ever before. This is primarily due to conceptual advances that have added the dimension of history to traditionally ahistorical fields such as behavior, ecology, and physiology. These advances have turned the dichotomy in to a trichotomy:
Structure vs. Function vs. History
The adaptation controversy revolves around a fundamental conflict between the teleological philosophy of Aristotle and the essentialism of Plato. A pivotal instance of the conflict was that of Georges Cuvier (comparative anatomy) vs. Etienne Geoffroy St. Hiliare (morphology). In 1830 a famous debate took place between Cuvier and Geoffroy. The main point of the debate was whether the explanation for the origin of form lies in teleology or homology.
I will first set the historical stage for the debate between Cuvier and Geoffroy in France, and then discuss the issues of the debate. The debate is particularly interesting because it involved the primary issues that Darwin tried to resolve in Britain. After establishing the connection between the CuvierGeoffroy debate and Darwinism, I will show that the issues are still not resolved in 1995. There is a fundamental split in biology that has its roots in greek philosophy and 17th century theology that continues to generate controversy today.
The idea of adaptations, or features that suit organisms to their environments is an old one. The Greeks had three explanations for adaptations, or progress in nature
These are fundamental issues, that in various forms have been debated for over 2000 years. The Greeks, and the philosophers of the Enlightenment thought deeply about these issues, and even with the increased understanding that modern science has given us today, they are not yet resolved.
Aristotelian physics was generally accepted during the Middle Ages -even purely physical processes were explained as a means to an end. The universe was a system of connected adaptations, and any natural process implied a designer.
Adaptation (= contrivance) = structure or process fitted to a specific function or goal.
Christian Theology
Theism - The Classical position of Providence: God created the world, and continues to guide its progress.
Classical theism became more and more complicated in the explanation of natural phenomena during the expansion of scientific knowledge during the Enlightenment. Deism allowed for natural processes independent of the adapting hand of God (but not the intending mind).
Deism - God created natural laws that govern the world. Religious doctrine has no place in science (Laplace).
Arguments of Design (John Wells, UC Berkeley)
Argument from Design:
If Design exists, then God exists
Design exists, therefore God exists
The argument from design (Thomas Aquinas) has had little role in christian theology, with two exceptions: (British, Protestant) Natural Theology, and modern "Scientific" Creationism. In contrast, the argument to design is central to christian theology.
Argument to Design:
If God exists, then Design exists
God exists, therefore Design exists
If design did not exist, this would refute the existence of God! So Design is central to the theological controversy over Darwinism.
The arguments of design are indirectly related to what many see as the fundamental dichotomy of biology: that of Functionalism and Structuralism.
Functionalism
Teleology -each structure has a function, or reason for being. (Teleology = study of ends or goals)
There is evident design in nature.
Form follows function.
Structuralism
The British School - Natural Theology
Paley's argument: if we come upon a watch, there is no doubt that it is a product of design; the intricate and intentional design implies a designer. How much more do the complex adaptations of animals imply an omnipotent and benevolent Creator!
"In crossing the heath, suppose I pitched my foot against a stone, and were asked how the stone came to be there, I might possibly answer, that, for any thing I knew to the contrary, it had lain there forever... But suppose I had found a watch upon the ground, and it should be inquired how the watch happened to be in that place, I should hardly think of the answer which I had given before... Yet why should not this answer serve for the watch, as well as for the stone? ...in the watch...are seen contrivance, design; an end, a purpose; means for the end, adaptation to the purpose. And the question which irresistibly presses upon our thoughts, is, whence this contrivance and design. The thing required is the intending mind, the adapting hand..." (Paley 1802)
Paley's argument is the argument from design to God. It relies on evident or perceived design, and an implicit relationship between design and a designer.
David Hume (1748, An inquiry concerning human understanding) attacked the argument from design. Most philosophers consider his work to be the end of the argument from design. However, I will show that it lives on today in another form...
"When we infer any particular cause from an effect, we must proportion the one to the other and can never be allowed to ascribe any qualities but what are exactly sufficient to produce the effect. ...if we ascribe to it further qualities or affirm it capable of producing other effects, we can only indulge in the license of conjecture and arbitrarily suppose the existence of qualities and energies without reason or authority." (Hume 1748, P.145-6)
The message here is that the product, say the eye, only requires a causal (and perhaps internal and organismal) process sufficient to produce an eye not an omnipotent, benevolent, Creator, who has continuing involvement in the world. Any speculation beyond that is just speculation.
The French School - the CuvierGeoffroy debate
In moving across the English Channel to France, I should mention that there was obviously much more going on in continental Europe in the early and mid 19th century than I can discuss today such as the rise of materialism in Germany. E.g. Müller, Schwann.
Georges Cuvier was a comparative anatomist, and one of the founders of paleontology. He was extremely influential in 19th century french academia, and was called the "legislator of science". He strongly rejected the transformism of Lamarck, and while he avoided discussion of religion in his writing, he was devout.
Key points about Cuvier:
Etienne Geoffroy was a student of the work of the french naturalist, Buffon. Buffon was a deist. Buffon also had the idea of common descent by degeneration and adaptation to the environment! Buffon was not an advocate of Linnaen taxonomy, and believed only in species as real entities, with a continuity of gradation. Geoffroy went on to the Academy of Sciences in Paris, where he interacted closely with Cuvier.
Key points about Geoffroy:
An example of Geoffroy's homology is the furcula (wishbone) which was thought to be restricted to birds, and to have a major functional role in flight. Geoffroy identified a homologous furcula in fishes, and postulated that the bone changed function as it passed from one class to another. This was an example of "the tendency of nature to cause the same organs continually to appear in animals formed on the same type." So, the furcula was not specifically designed by God for flight in birds (as claimed by Cuvier), but instead an abstract element of organization that could have different functions in difference species.
Points of Conflict
The debate was a public one, and began in a friendly way. In the end both Geoffroy and Cuvier agreed to end it because things were becoming too heated. Cuvier was the better anatomist, and presented his arguments in a more logical way. He showed organs present in mollusks and not in vertebrates. However, Geoffroy used the hyoid bones in vertebrates to demonstrate his principle of homology. The hyoid is part of the gill skeleton in fish, part of the tongue projection aparatus in plethodontid salamanders, and part of the hyoid is in the inner ear of mammals (as well as in the throat). But Cuvier continued to emphasize the dissimilarities, rather than the similarities. So, while teleology seemed to win out in the debate, this is in some ways misleading. Comparative anatomy was greatly changed, and homology became an integral part of it. It became accepted that unity of plan often transcended similarities of function.
The British School, after the debate
Owen (1843) attempted to synthesize teleology and morphology.
He made an argument for homology: man-made machines are adapted solely as means to an end. Humans do not constrain design according to a common plan (but maybe they do: e.g. architecture during the art deco or art nouveau periods was constrained by rules of structure).
"There is no community of plan or structure between the boat and the balloon, between Stephenson's locomotive engine and Brunel's tunnelling machinery: a very remote analogy can be traced between the instruments devised by man to travel in the air and on the sea, through the earth or along its surface. The teleologist would rather expect to find the same direct and purposive adaptation of the limb to its office as in the machine." (Owen 1843)
Instead, the limbs of volent, terrestrial, fossorial, and aquatic vertebrates share a common structure; that is, they are homologous.
It is in divergence from the Archetype that there is a role for teleology: Owen saw differences among homologous structures as adaptive specializations of a generalized, primitive Archetype. For example, the "lowest" were not far removed from the Archetypical (or Platonic Ideal) vertebrate. Teleological modifications of the Archetype take the form of a Scala Naturae, with the highest rung reserved for man.
"The recognition of an ideal Exemplar for the Vertebrated animals proves that the knowledge of such a being as Man must have existed before Man appeared. For the Divine mind which planned the Archetype also foreknew all its modifications." (Owen, On the Archetype and Homologies of the Vertebrate Skeleton, 1848)
Darwin
Darwin began as a Deist. On Geoffroy St. Hiliare "H. says grand idea God giving laws and on them leaving all to follow consequences." (Darwin 1837) However, like most of the British school, he was also a teleologist. He was strongly influenced by Owen's synthesis of teleology and morphology.
"It is generally acknowledged that all organic beings have been formed on two great laws -Unity of Type, and the Conditions of Existence. By unity of type is meant that fundamental agreement in structure which we see in organic beings of the same class, and which is quite independent of their habits of life. ...unity of type is explained by unity of descent. The expression of the conditions of existence, so often insisted on by the illustrious Cuvier, is fully embraced by the principle of natural selection. ...in fact, the law of the Conditions of Existence is the higher law; as it includes, through the inheritance of former variations and adaptations, that of Unity of Type." (Darwin, 1859)
Darwin strongly rejected the arguments of Paley, but Asa Gray at Harvard (1860) was Darwin's theory as support of the argument from design. Gray cited,
"Darwin's great service to natural science in bringing it back to Teleology: so that instead of Morphology vs. Teleology, we shall have Morphology wedded to Teleology."
Gray and Darwin were friends, and Gray was probably joking when he said it, however Darwin responded in a personal letter,
"What you say about Teleology pleases me especially, and I do not think any one else has ever noticed the point. I have always said you were the man to hit the nail on the head." (Asa Gray and C. Darwin in Wells, J. 1988. Charles Hodge's crituque of darwinism. Studies in American Religion. Edwin Mellin Press, Lewiston.
This represents a semantic transformation of theusage of Design. Darwin continued to reject any notion of Theistic Design. In response to Gray and his idea of derected, beneficial mutation, he said,
"An omniscient Creator must have foreseen every consequence which results from the laws imposed by Him. But... Did he ordain that the crop and tail feathers of the pigeon should vary in order that the fancier might make his grotesque and fantail breeds? ...-no shadow of reason can be assigned for the belief that variations, alike in nature and the result of the same general laws, which have been the groundwork though natural selection of the formation of the most perfectly adapted animals in the world, man included, were intentionally and specially guided." (Darwin 1896, The variation of animals and plants under domestication. Pp. 427-8)
However, Darwin changed nothing in that his theory still depended on teleology. In discussing pollination in flowering plants, he wrote about "...an inexhaustible number of contrivances, all for the same purpose and effected in essentially the same manner..." (Darwin 1959, P142). Natural selection is substituted for God as the mechanism of Design. This is a profound difference from a theological viewpoint, but the semantic form of the argument is similar.
Darwin had two types of arguments for natural selection as the origin of form and function.
E.g. Because artificial selection can use the accumulation of small inherited variations to produce dramatic results, the analogous process of natural selection, given a great amount of time, could produce, say, an eye or a hand.
If Design Þ N.S. for it made it so
Design N.S. for it made it so
E.g. It is evident that the function of the eye is sight. Natural selection for sight must have acted on chance variations to produce increasingly optimal eyes.
The specific explanation is the most clearly teleological, since requires evident design, and the action of a goal-directed process.
On the other hand, Darwin clearly emphasized the use of homology in comparative biology.
"In searching for the gradations through which an organ in any species has been perfected, we ought to look exclusively at its lineal progenitors; but this is scarcely ever possible, and we are forced to look to other species and genera of the same group, that is to collateral descendants from the same parent-form, in order to see what gradations are possible..." (Darwin 1859)
So Darwin left us largely where we began: can we simply look at the "function" of a feature and know how it came to be? Or do "rules" of structure govern form?
Teleology and Homology Today
Adaptationism - Modern Teleology
"It was the daily, indeed hourly, scrutiny of natural selection, as Darwin had said, that inevitably led to ever greater perfection. Ever since then it has been considered one of the major tasks of the evolutionist to demonstrate that organisms are indeed reasonably well adapted, and that this adaptation could be caused by no other agency then natural selection."
Lewontin (1980) Gould &;Lewontin (1978): criticized the "adaptationist programme" for its failure to distinguish current utility from historical origin, and its reliance on natural selection as the only important factor in evolution. They quoted Voltaire's fictional character, Dr. Pangloss (all tongue),
"Things cannot be other than they are...Everything is made for the best purpose. Our noses were made to carry spectacles, so we have spectacles. Legs were clearly intended for breeches, and we wear them." (Gould and Lewontin 1979)
Adaptive stories often postulate a perceived fitness advantage or optimal design as the reason for being. Because it often depends on a thought experiment, this could be derisively called the "Kipling approach", after Rudyard Kipling's Just So stories. However, this approach has been extremely popular -especially in the fields of behavioral ecology, sociobiology, comparative physiology, and functional morphology. Gould and Lewontin used a non-biological example to show how a seemingly useful character that shows evident design could be an epiphenomenon: is it purposful design or a byproduct of the arcitectural plan?
The human chin -is it a character -a thing? Gould and Lewontin claimed not, since it is a byproduct of the alveolar and mandibular growth fields in development.
For example, the recent discovery of an early fossil whale with small but complete hind limbs has raised speculation about their function. They could have been for copulation, or for maneuvering in shallow water. (On the other hand, didn't the ancestors of whales have hind limbs?)
Gould &;Vrba (1982): proposed the term, exaptation, to distinguish a feature that arose by natural selection in a different role than it currently holds. For example, since wings in birds arose in the context of flight, they are exaptations to swimming in penguins. Exaptation is based on homology.
Greene (1986) outlined a methodology for testing adaptational hypotheses based primarily on homology. This method looks for concordant homologies in form and function. I will talk in detail about this in the next lecture.
The debate continues, and a recent article by Reeve and Sherman (1993, Q. Rev. Biol. 68) argues that history (homology) is irrelevant to adaptation.
"...an intricate fit between form and function could arise only through natural selection, and not through random processes... For example, the optical designs of eyes approach theoretical optima predictable from physics... it seems inconceivable that these designs are not adaptations produced by selection."
(If you substitute NS for Design, this quote could just as well have come from Paley!)
Reeve and Sherman's methodology -basically the adaptationist programme in its most extreme form: the point is to answer a "why" question a narrative consistent with N.S.. This is basically a plausibility argument.
Reeve and Sherman give an alternate interpretation of Halliday and Arnold's work on multiple matings (polyandry) in females. Halliday and Arnold postulated that polyandry could be best explained by direct selection for polygyny in males, and by a genetic correlation between male and female behavior. They criticize Halliday and Arnold for an incomplete phenotype set. Because there is evidence for a genetic correlation between polygyny and polyandry, they infer that selection might have favored the correlation and the independent traits.
In another instance, Reeve and Sherman criticize Wake's (1991) claim that developmental constraints can produce seemingly convergent evolution (see the Wake 1992 article in reader). Wake's argument for 4 and 5-toed plethodontid salamanders was based on the effect of body and genome size on the number of cells in the primordial limb buds. Selection for very small body size may pleiotropically result in digital reduction. Relatively unrelated species could exhibit "convergence" or homoplasy in having 4 toes, but this would not necessarily be due to a selective advantage of 4 over 5 toes.
Reeve and Sherman's criticisms:
"Since Wake offers no evidence of the relative fitnesses of small four-toed and five toed individuals within plethodontid taxa, design constraints offer at best a description, not an explanation, of the occurrence of four-toedness."
Perhaps four-toedness is more optimal for clinging and climbing in small salamanders.
Finally, George Lauder, in a recent TREE article argued that it is methodologically impossible to determine the past action of natural selection on a character for and only for a given function. In this somewhat pessimistic paper, he suggests that any historical (homology-based) approaches to adaptation are futile.
Whild I disagree with his conclusion, I agree with Lauder that it is not possible to know how selection has acted in the past, and it is clear that all of the methodologies for studying adaptation are better at rejecting the hypothesis of adaptation than accepting it (as in inferential statistics, one can never accept the null hypothesis). I think Reeve &;Sherman, and many others would disagree with me on that point because they see natural selection as a predicable process. This boils down to a difference between two world views -necessity and contingency. As scientists, it is our job to determine which viewpoint is the more valid in any given situation..
Other References
Appel, T.A. 1987. The CuvierGeoffroy debate: french biology in the decades before Darwin. Oxford Univ. Press, N.Y., N.Y.
Darwin, Charles. 1859. On the origin of species. A facsimile of the first edition. Harvard Univ. Press, Cambridge, Mass., 1964.
Gould, S.J. 1993. The gift of new questions. Natural History 8/93:4-13.
Lull, R.S. 1925. Organic evolution. MacMillan, N.Y.