Evolution Is More Than Natural Selection

Developmental systems may have many potential outcomes, some of which may turn out to be adaptations only "after that fact." While evolution can thus occur with or without natural selection, the really big transformations are unlikely to have been produced by incremental adaptation.
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dna structure
dna structure

The notion that some organisms are better suited for life than others, and that the successful ones tend to prevail over the less successful ones, is ancient folk wisdom, not an original idea of Charles Darwin's. No one disagrees with this, including creationists, who nonetheless deny that this kind of selection leads to large-scale, "macroevolutionary" changes (e.g., differences between frogs and flies). Darwin's concept of "natural selection," in which macroevolution is just the result of microevolution (selection of incremental function-related differences) occurring over many generations, is only one of several theories of how differential survival has led to the diversity of life, but one that has been largely unchallenged until recently. Although these are straightforward distinctions, it is a longstanding maneuver of proponents of the natural selection-based "modern evolutionary synthesis" to associate criticism of their theory with creationism and irrationality.

One symptom of the unraveling of a scientific paradigm is that its advocates tend to change the subject when their favored views are criticized. A recent blog post of mine that suggested that the physics of embryonic development can tell us something about why complex organisms have the characteristic forms they do, and explored how this might shed light on the origin of the major types of animals and plants, was subjected to this kind of feint at the blog site of evolutionary biologist Jerry Coyne. A University of Chicago professor and a self-acknowledged defender of the Darwinian synthesis against "contrarians, creationists, and those who know little about evolution," Coyne wrote in response to my post, "I haven't seen anything that makes me think that natural selection is an outmoded way to think about the evolution of adaptations."

"Adaptation" as an organismal feature is a concept that emerged essentially coincidentally with Darwin's theory of evolution. For example, Wikipedia defines "adaptation" as "a trait with a current functional role in the life history of an organism that is maintained and evolved by means of natural selection." This would make Coyne's assertion true by definition. If we cut off the description at the word "organism," however, we get a definition that does not presuppose natural selection. This is the approach that Coyne was apparently taking, though it is difficult not to conclude that his terms of reference are theory-laden. I did in fact use the term "adaptation" in my post, but only to indicate that it was not what I was discussing.

Should adaptations even be at the center of a theory of evolution? There are certain things that come along with being a material object (having mass and the capacity to absorb heat, for example) that are properties of every biological system, and even required for life, but which no one would think of calling "adaptations." There are even things more specific to living systems (e.g., the ability to generate heat and carbon dioxide, the requirement for water, etc.) that also are not adaptations. Most evolutionary biologists would search for adaptations among features characteristic of living systems that are optional -- that is, features that distinguish one organism or type of organism from another but, like the above "generic" features, can be passed from one generation to the next. But are all such distinguishing features adaptations? Not really. That concept seems to require an associated function. My ears have some similarities and some differences in shape compared to those of both of my daughters. Such things are undoubtedly inherited, but they don't seem to fit the definition of an adaptation.

So far we have been considering a world of variable living organisms in which adaptations are not that important. But some things obviously fit the definition of "adaptation" as having "a current functional role in the life history of an organism" and which unquestionably have evolved to assume that role -- my bipedal stance, for instance. This character was not present in my primate ancestors, and it confers a tremendous advantage to me in my everyday life. There is a whole suite of anatomical novelties associated with human bipedality (and that of other bipedal tetrapods, such as kangaroos and birds), including novel insertions of tendons and ligaments between thigh muscles and pelvic and limb bones, that are correspondingly differently shaped in bipedal animals compared with their quadrupedal ancestors.

Scenarios for the emergence of bipedality in humans include increased efficiency of traveling or eating; acquisition of a sexual dimorphism in resource gathering and provisioning of food, leading to monogamy and pair bonding; evasion of predators; and ability to transmit warning displays. These proposals were all made in the context of the standard evolutionary framework, with the implied requirement of many cycles on incremental variation and reproductive competition, in recognition of all the anatomical modifications required to arrive at a recognizably bipedal state. As Richard Dawkins asserts (rather agitatedly) in the comments section of the aforementioned blog entry by Jerry Coyne, "[N]atural selection is the ONLY thing that can explain ADAPTATION."

But is this the case? In 1942 E. J. Slijper described a goat born without forelegs that learned to get around by hopping on its hindlegs like a kangaroo. Having met with an accidental death at 1 year old, it was dissected and found to have had a musculoskeletal system with a number of features not characteristic of goats but similar to ones found in bipedal mammals (Slijper, 1942). So not only was it efficiently bipedal, but it had the underlying morphological adaptations associated with this condition. But this bipedality occurred suddenly, as a "saltation" or jump.

Defenders of natural selection as the exclusive mechanism of macroevolutionary change will say:
  1. "Darwin acknowledged such rare occurrences, calling them 'sports.'" Yes, but he dismissed their role in evolution, as did R. A. Fisher, who formulated many of the mathematical arguments underlying the modern synthesis.
  2. "We don't know whether the body form of Slijper's goat was heritable." True, but the observation indicates that bipedality is a "plastic" response of the pre-natal (or more likely post-natal) musculoskeletal developmental system that, in conjunction with its own initiative and survival instinct, allows an organism with no forelimbs, or with impaired forelimbs, to invent a satisfactory mode of life in the space of a single generation.
  3. "If a phenotype is an adaptation, then you still have to invoke natural selection as a cause of the corresponding patterns (i.e., the particular evolutionary process that has altered the genes to produce such patterns)." Jerry Coyne actually said as much in the blog post linked to above. But this statement implies the belief that the evolutionary history of four-legged animals included selective regimens (based on genetic variation and competition among variant organisms) that ensured that if one of their descendents was ever faced with missing forelimbs, it had a genetic program in reserve to produce a functional hopping animal, with preprogrammed musculoskeletal specializations to facilitate this mode of life. All this just to preserve the idea that everything significant about the differences among organisms are adaptations, and that such adaptations cannot evolutionarily precede the naturally selected (i.e., based on functional utility) "genetic programs" that generate them. The alternative is to recognize that developmental systems have many potential outcomes, some of which may turn out to be adaptations only "after that fact." If some morphological novelty finds a new use, it will be retained if the precipitating cause, which might be mutational or environmental, is perpetuated. If not, then it will not be retained. (Biologist Richard Palmer considers the asymmetrical positioning of the heart to be an example of this [Palmer, 2004].)

While evolution can thus occur with or without natural selection, the really big, phylum-defining transformations, which happened in an era when developmental systems were much more plastic than they are now, are unlikely to have been produced by incremental adaptation-based mechanisms. I hope to discuss these early phylogenetic events in a future blog post.


Palmer, A.R. (2004) Symmetry breaking and the evolution of development. Science 306: 828-833.

Slijper E.J. (1942) Biologic-anatomical investigations on the bipedal gait and upright posture in mammals, with special reference to a little goat, born without forelegs. Proc. Koninklijke Nederlandse Akademie Van Wetenschappen 45:288-95, 407-15.

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