When I was contacted to write an article for the "Six papers that shook..." column of Porcupine!, I was first curious about why the number should be six instead of other numbers. The column title suggests that the number five or seven, or any other number, is less optimal than number six in most cases based on certain criteria. Have other numbers been tried before and found undesirable? Has there been a competition among numbers with this magical number six gradually emerging as a winner?

There might well be a nice story behind this number six, or there might be no story at all. However, even if there is no story behind the number six, people driven by curiosity and gifted with imagination will come up with some stories in the future and the story, if well told, will be gradually taken as truth.

The field of evolutionary biology is full of story-telling geniuses, whose stories have plagued the mind of many, especially those like me who are fond of good stories. Eventually the story will be built up to such a grandiose scale that a phenomenal effort will be needed to dismantle it. The phenomenal effort, when expressed in a publication, will then be called a classic.

One such classic is George C. Williams' 1966 book, Adaptation and natural selection: a critique of some current evolutionary thought, which I read when I was doing field work on the deer mouse populations in the Kananaskis Valley in the Canadian Rockies, in the summer of 1985. The Environmental Research Center of the University of Calgary, where I stayed during the summer of field work, has a nice library with quite a number of classics in evolutionary biology, including this classic by Williams. The book contains pointed criticisms of misinterpretations of Darwinian theory of natural selection by a number of leading evolutionary biologists. It was written in such a powerful, spirited and persuasive manner that my heart was beating extraordinarily fast when reading the book. I have since become much more critical than before, both of other people's works and of my own.

The second classic that influenced (or "shook") me greatly is John Maynard Smith's 1978 book The evolution of sex, which I read in 1989. At that time I had already finished reading G. C. Williams' 1975 book Sex and evolution, and perhaps most other publications by Williams. Because of my admiration of Williams' writings, I was almost infuriated to find someone writing on the same topic. How could anyone even dare to think that he had something to add to what Williams had just written on? I therefore read the book very critically, and consequently progressed rather slowly, trying to find flaws. Yet there is no flaw throughout the entire book, except for a very minor one close to the end of the book, which I mentioned in American Naturalist in 1992. The book contains so many ingenious ideas presented in such a lucid manner that, in my opinion, it is not rivalled by anyone, not even Williams. I have since learned that Maynard Smith had criticized group selection even before Williams, developed the concept of evolutionary stable strategies and also served, albeit for a short time, the devil's advocate in the selectionist-neutralist debate in the development of the neutral theory of molecular evolution. It is in fact through an early article by Maynard Smith that I began to learn about the debate, and it is a publication that emerged from the debate that I will now introduce as my third classic that "shook" me. But first let me give you a partial background to set the stage of the debate.

According to the neo-Darwinian theory, mutation is the ultimate source of genetic variation, which is true, but natural selection is given the dominant or "creative" role in shaping the genetic makeup of populations. Most mutations were thought to be mostly deleterious, but occasionally advantageous mutations would arise, and gene substitutions would occur as a consequence of selection of advantageous mutations. Two populations of the same species in two different environments would diverge genetically because natural selection would favor different genes that were good for their respective environments. This scenario led to two predictions. The first is that most genetic differences between populations or species are those with important phenotypic manifestations. The second is that the gene substitution rate should be low. This second prediction may not be immediately obvious to you if you have not heard of the substitution load. So we digress a bit further.

The substitution load was previously termed "the cost of natural selection" by J. B. S. Haldane. If natural selection is to improve the population, or at least maintain the population in its current status of adaptation, it has to eliminate those individuals carrying deleterious mutations. To fix a new advantageous gene, the population has to go through the selection process in which all individuals not carrying the new advantageous gene would be eliminated, which is "costly" indeed to the population. This implies that gene substitution by natural selection favoring advantageous genes is a very slow process. Hence the second prediction that gene substitution rate should be very low.

These two predictions, which seem highly plausible if not obviously correct, turned out to be wrong. The gene substitution rate, when quantified at the molecular level, was found to be much higher than previously expected based on the neo-Darwinian theory. Thus the second prediction of the neo-Darwinian theory fails. The first prediction, that gene substitution was mainly through natural selection favoring advantageous genes, and that genetic differences between populations or species should mainly be reflected in those genes correlated with fitness, fails just as badly. Most substitutions are "silent" (or neutral) at the molecular level and have no bearing on fitness, and most differences among populations or species are made of such neutral differences. These observations, as well as many others, accord well with the predictions of the neutral theory, but not with the neo-Darwinian predictions.

The neutral theory is one of the few evolutionary theories that greatly influenced how molecular biologists go about their research. If molecular biologists want to find important genes, or important segments of a gene, then they should look for conserved genes or gene segments, i.e., those that are the same in mice and frogs, rather than looking for those highly variable genes or gene segments.

The neutral theory of molecular evolution by Motoo Kimura (1983) presents the conceptual framework of the theory as well as empirical evidence in support of the theory. To my understanding, the book is flawless except for a very trivial one on the evolution of codon usage in protein-coding genes, which I mentioned in Genetics in 1998. It is through reading this book that I truly appreciate Th. Dobzhansky's proclamation that "Nothing makes sense except in the light of evolution".

Now I have to challenge again the wisdom of choosing the number six. According to Dr. Corlett, the "Six papers..." article should be just about one page long. I have now covered just three publications and the article on the screen is already creeping into the third page. This is already my second attempt at limiting the article to one page, and now I have no alternative but to admit a total failure.


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