The Frailty of the Darwinian Hypothesis, Part 1
Editor's Note: Ann Gauger is a senior research scientist at Biologic Institute. Her work uses molecular genetics and genomic engineering to study the origin, organization and operation of metabolic pathways. She received a BS in biology from MIT, and a PhD in developmental biology from the University of Washington, where she studied cell adhesion molecules involved in Drosophila embryogenesis. As a post-doctoral fellow in the Department of Molecular and Cellular Biology at Harvard, she cloned and characterized the Drosophila kinesin light chain. Her research has been published in Nature, Development, and the Journal of Biological Chemistry. Her awards include a National Science Foundation pre-doctoral fellowship and an American Cancer Society post-doctoral fellowship.
A long-standing controversy exists among evolutionary biologists that is little known outside of professional journals. This controversy is significant because it deals directly with the question of how evolutionary processes produce functional changes in organisms --- whether or not the changes we observe are due to adaptive processes guided by natural selection.
Why such a controversy? In his landmark book On the Origin of Species, Darwin proposed natural selection as a force sufficient to account for the organismal complexity and diversity we see around us today. But Darwin knew nothing about genetics or molecular biology. He knew nothing about how variation among organisms was produced or inherited, or what the limits of variation might be. He knew nothing about population dynamics or how difficult it might be for a slightly advantageous trait to spread throughout a population.
In the many years since Darwin wrote his book, scientists have learned much about these topics, and as a result, they have identified four forces driving evolution, not just the one known to Darwin. The four forces are natural selection, mutation, recombination, and genetic drift, and when taken together they affect evolving populations of organisms in sometimes surprising ways. This has led to the controversy I outlined above concerning the efficacy of natural selection to drive evolution in adaptive directions.
Let me explain what the four forces are, and then I will describe the problem they pose.
Natural selection is the evolutionary force with which most people are familiar, and can be simply stated as follows: organisms better adapted to their environment tend to survive and have more offspring than other less fit counterparts, all other things being equal. Mutation and recombination act as the engine of organismal variation: mutations change an organism's DNA (by substitution, insertion or deletion of particular bases, or modification of the DNA), while recombination shuffles the DNA into new combinations, thus producing further variation. This means that each individual has a unique genome. Differences in each individual's DNA can produce differences in how well the organism functions in its environment. Finally, genetic drift causes particular variations to be lost from small populations at random, simply because individuals may die or fail to reproduce for reasons unrelated to their fitness for their environment.
It is important to note that three of these four evolutionary forces are non-adaptive and stochastic. An evolutionary force is considered non-adaptive when the change it produces is independent of whether it confers a benefit. It is stochastic when its occurrence is randomly distributed, and cannot be precisely predicted. We can say something about how frequently a stochastic event is likely to occur, but we cannot say what specific changes will occur.
With regard to the above evolutionary forces, this means that mutations occur at random, independent of whether they help or harm, and recombination occurs at random, whether or not it produces helpful or harmful new combinations of genes.1 Similarly, genetic drift increases the likelihood that a potentially beneficial mutation will be lost before it becomes widespread in the population. This is particularly true for organisms with small effective population sizes, such as vertebrates. The net effect of genetic drift in such populations is "to encourage the fixation of mildly deleterious mutations and discourage the promotion of beneficial mutations,", in the words of one evolutionary biologist.2 Only natural selection is adaptive, that is to say, working to ensure that beneficial changes are preserved in the population, and harmful changes are eliminated.
This may seem counter-intuitive, so let me reiterate this point. Because of the accidental effects of genetic drift in small populations, natural selection is not strong enough to guarantee that beneficial mutations will eventually become fixed (universal) in a population or that weakly harmful mutations will be eliminated. Thus, in organisms with small effective population size (e.g. all vertebrates, which includes us humans), the stochastic and non-adaptive forces of mutation, recombination, and drift will tend to drive evolution in non-adaptive directions.
We see the powerlessness of natural selection to eliminate harmful mutations quite clearly, with the variety of hereditary diseases that exist in human populations today. Extremely harmful dominant mutations that cause death immediately, or prevent reproduction, do not spread in the population. However, less immediately harmful dominant mutations, such as those that cause Huntington's Chorea, permit survival into and past the reproductive years and so are not eliminated. Recessive mutations, like those causing sickle cell anemia or cystic fibrosis, can be present at substantial levels in the population, because having one mutated gene copy has little or no effect on an individual. Only when someone inherits a bad copy from both mother and father do they develop the disease.
And new mutations happen all the time, most of which are either neutral (having no effect), or harmful (causing varying amounts of damage or disease).
What about the rare beneficial mutations? Once again, unless the benefit is very strong, and confers a very large advantage to the individual carrying the mutation, it may never spread through the population. An example here might be the ability of Northern Europeans to digest milk as adults. This ability arose when a mutation allowed an enzyme that digests milk to be produced in adults, and not just in infants. This is a simple advantageous mutation for milk drinkers, but it is not universal among humans, as any one with lactose intolerance can tell you. And it may never be universal, because the selective advantage of being able to eat dairy products is not large unless your diet depends exclusively on milk products for most of the year.
This picture of evolution is strikingly in contrast to the stories told by biologists who believe in the adaptive power of natural selection to generate whole new cellular systems, behaviors, and body plans (see for example Endless Forms Most Beautiful by Sean Carroll 3 or most evolutionary psychology arguments 4). If three out of the four forces driving evolution are non-adaptive, then perhaps most evolutionary change is also non-adaptive, and not due to the power of natural selection. Hence the controversy.
In the next post I will consider some of the implications of this controversy for intelligent design theory.
1 This is the standard story. Some scientists are now proposing that mechanisms exist to promote targeted mutations when organisms are stressed [see for example Rosenberg SM (2001) Evolving responsively: adaptive mutation. Nat Rev Genet 2:504-15]. This idea remains highly controversial. If true, the resulting mutations would occur at a higher frequency in the targeted gene(s), but should still be stochastic in nature, and without regard to adaptive benefit.
2 Lynch, Michael (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci USA 104:8597-8604.
3 Sean Carroll (2005) Endless Forms Most Beautiful. WW Norton and Company, New York.
4 See for example: http://www.epjournal.net