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1 1 Lecture 9 The neutralist - selectionist controversy Looking back, I think that it is a curious human nature, that if a certain doctrine is constantly being spoken of favorably by the majority, endorsed by top authorities in their books and taught in classes, then a belief is gradually built up in one's mind, eventually becoming the guiding principle and the basis of value judgement. At any rate, this was the time when the panselectionist or 'neo-darwinian' position was most secure in the history of biology: the heyday of the traditional 'synthetic theory' of evolution. (p22) The neutral theory of molecular evolution by Motoo Kimura, Cambridge University Press, 1983, reprinted 1986 (paperback), 367 pages Contents: 1. From Lamarck to population genetics Overdevelopment of the synthetic theory and the proposal of the neutral theory The neutral mutation-random drift hypothesis as an evolutionary paradigm Molecular evolutionary rates contrasted with phenotypic evolutionary rates Some features of molecular evolution Definition, types and action of natural selection Molecular structure, selective constraint and the rate of evolution Population genetics at the molecular level Summary and conclusion References Kimura s work will show that a critique of Darwinism is possible, without being ridiculed or ignored by the scientific community. His Neutral Theory got a firm place in the standard textbooks on evolution and population-genetics, despite being clearly anti-selectionist. In the beginning orthodox Darwinists did not exactly like Kimura s theory, because he was telling the scientific community that all powerful Natural Selection was not so powerful after all. Natural selection had its limitations. On the molecular level the power of Natural Selection was greatly minimized, if not banished at all. Randomness took its place. Molecular variation in proteins and DNA was uncovered that had no influence on the fitness of the individual organism: in other words: is selectively neutral. On could even doubt if Natural Selection was of any importance in the traditional areas of morphology and anatomy. Why did Kimura find its place in evolution textbooks, unlike other anti-darwinists? The growing evidence supporting the Neutral Theory The Neutral Theory made a lasting contribution to population genetics theory Kimura built his theory on accepted knowledge in genetics and population genetics and at the same criticized it and extended it Kimura did not deny the existence of natural selection on morphological levels Kimura shows that critique of neo-darwinism can be incorporated into neo-darwinism if there is evidence and a good theory which contributes to the progress of science. Were neo-darwinists really opposed to neutralism around 1970? Consider Ernst Mayr s Populations, Species, and Evolution (1971). After summarizing the evidence for genetic drift ( King and Jukes(1969), Kimura(1969), Fitch and Margoliash(1970).), Mayr notes that a number of considerations largely deprive the evidence of its cogency: There are several other properties of populations that, when only superficially analyzed, appear to have no obvious selective advantage. However, the mere fact that such traits have become established makes it highly probable that they are the result of selection. More and more sites even in the largest molecules are found to have specific functions. A functionless site is simply one the function of which has not yet been determined. Available observations on allele polymorphism are not consistent with the neutrality theory.

2 2 A random replacement of amino acids unquestionably occurs occasionally in evolution, but it appears at present that it does not anywhere near approach selection in importance as an evolutionary factor. Chance causes disorder, selection causes order. It is clear from the first two points that Mayr treats function and natural selection virtually as an axiom. So neutralism is almost excluded by definition. The other points concern evidence. Much evidence has been produced since 1970, but in 1982 Mayr still concludes: My own feeling is that selection is far more important than admitted by the promoters of non-darwinian evolution, but that indeed there is a random component in much of the variation at some gene loci. So according to Mayr(1982) selection is still more important than neutral mutations or Random-Walk Evolution as he calls it. Notes. 1. This book is not available anymore from the publisher, but there is a collection of papers by Kimura: Population Genetics, Molecular Evolution, and the Neutral Theory: Selected Papers, University of Chicago Press, (The essays cover 40 years of Kimura's contributions to the understanding of how genetic variation affects evolutionary change). 2. There are 15 publications of Kimura listed in the bibliography of Hartl and Clark s Principles of Population Genetics(1997). 3. Second printing 1971, pages 117 and 127,128. This is the abridgement of Animal Species and Evolution,1963, Ernst Mayr: The Growth of Biological Thought. Diversity, Evolution and Inheritance., 1982, page 593. NEUTRALIST* SELECTIONIST ELECTROMORPHS / ALLOZYMES (ALLELES) ARE MOSTLY SELECTIVELY NEUTRAL TRAITS OF NO SELECTIVE OR PHENOTYPIC CONSEQUENCE This means that variation is irrelevant to a population's capacity to respond to new forces of selection. Genetic variants do not differ in fitness and do not constitute raw material for adaptation to new selective regimes. GENETIC DRIFT IS IMPORTANT IN DETERMINING FREQUENCIES OF NEUTRAL ALLELES AMONG GENERATIONS. This means sampling errors occur generation to generation because alternate alleles have identical (relatively neutral) fitnesses. Molecular evolution is mostly caused by drift. ALLELES HAVE PHENOTYPIC CONSEQUENCE S UPON WHICH SELECTION MAY ACT, EVEN IF EFFECTS ARE SMALL SELECTION IS IMPORTANT IN DETERMINING ALLELIC FREQUENCIES This means most evolution occurs via natural selection; selection is more important than drift in determining gene frequencies. VARIATION IS NEUTRAL VARIATION IS BENEFICIAL (Fisher's Fundamental Theorem of Natural Selection) The Neutral Theory In the 1960 s Kimura made the claim that most molecular evolution was the result of genetic drift, not selection. He based this assertion on four main observations that he felt could not be explained by natural selection, but could be explained by genetic drift of neutral mutations 1. The rate of evolution of proteins is too high, ~1 x 10-9 aa changes/aa/year 2. The rate is constant in different lineages 3. Different proteins, and different parts of the same protein, evolve at different rates with the least important evolving faster 4. The amount of heterozygosity and polymorphism is higher than would be predicted for directional selection If Kimura is correct then most changes at the molecular level are neutral and the rate of neutral mutations is high, if the selectionist are correct than most changes have a selective advantage and neutral mutations are rare The Rate is too High Haldane and the cost of selection also known as the substitutional load o The genetic load is the reduction in fitness caused by carrying deleterious alleles o If this effect is summed over the whole genome than there can only be a few such substitutions taking place at any

3 one time. 3 o Haldane calculated the top rate to be one substitution/300 generations Kimura estimated that at 3 x 10-9 aa changes/aa/year a new allele was being fixed every 2-3 years - 100x the rate Haldane had predicted o For the neutral theory the rate of evolution of neutral alleles is u, thus neutral mutation rates between 10-6 to 10-7 would explain the observed rate of mutation In addition, the neutral theory predicts the constant rate of evolution that is observed One problem - the rate should be constant over generations, not years (maybe the mutations are only slightly deleterious?) The Rate of Evolution is to Constant The molecular evolution rate is much more constant than the rate of morphological evolution Important Parts of Proteins (Active Sites, etc.) Evolve Slower than the less Important Parts Neutralist explanation: fewer neutral mutations in important areas Selectionist explanation: mutations in active sites are more likely to have a large effect, get fine tuning in less important areas o Kimura - while small s is more common they are also less likely to be fixed - cancels out Not true if the mutations can keep recurring Silent sites and pseudogenes evolve 5x faster than coding sequence o However, rates at silent sites do vary in different proteins o Also effected by codon bias The fact that there are mutations fixed at silent sites w/o a change in the protein suggest that the alleles are not identical by descent - uniformity is due to selection Silent sites do show a generation effect There is Too Much Heterozygosity The selectionist explanation for heterozygotes was heterozygous advantage Kimura showed that this could not be true because of the segregational load o In Drosophila 30% of loci are polymorphic and the ave. H is 10%, thus the polymorphic loci have an ave. H of.33 o If heterozygous advanatage is maintaining this than,for an average s of 0.1, the average fitness per loci is o If Drosophila has 10,000 genes than 3,000 will be polymorphic and the combined effect will reduce the average W to (1-(.33)(.1)) 300 = o This is ridiculous, therefore heterozygous advantage is not responsible for the observed heterozygosity For neutral mutations, u = 10-7 and N = 250,000 gives the 10% heterozygosty o The value for N seems too lo w (only 250,000 fruit flies?) and u seems to be too high - there should be more heterozygosity o Slightly deleterious mutations? The selectionist response o Kimura is confused about the difference between hard and soft selection hard selection increases the mortality in the population while soft selection only effects who is going to survive not how many

4 o Loci are not all independent 4 o Frequency dependent selection has no load Kimura was correct about heterozygous advantage not explaining the amount of observed heterozygosity. However, the connection between mutation rates and heterozygosity is still unclear Darwin Darwin 2 Fisher-Wright Fisher Mendel Wright Fisher Wright 2 1 Darwin Darwin A A Darwin Darwin Darwinian fitness

5 Darwin DNA

6 Hamilton H(q 1,...,q s ) Hilbert Hilbert Linear Operator dynamical state and property state Hamilton ultrafilter a map S t : X X (= a transformation of X into itself) (1) S 0 (x) = x, (2) S t (S t (x)) = S t+t (x) for t, t R. Markov 6

7 7 A a A a x y x y iff x y A a x x = {y y x} x A = {y & x A }, x a = {y y x & x a } x A x a = x A T(A) A a T(a) a A a x y iff x y AA Aa aa T(X) = X, X = AA X = Aa X = aa A a AA aa Coarse Graining (realization)

8 Gödel Leibniz (F)(Fx Fy) x = y x = y (F)(Fx Fy) x = y (F)(Fx Fy) x y iff x y x = {y y x} F( x ) Fy & x = y (F)(F( x ) F( y )) (intrinsic) (extrinsic) Ceteris paribus Ceteris Paribus Ceteris paribus

9 1 2 9 Ceteris paribus (special sciences) A. Ceteris paribus Ceteris paribus Ceteris paribus Ceteris paribus B. C. Ceteris paribus D. Ceteris paribus E : Rosenberg 2 :

10 One closed system Actual frequency Expected frequency Natural selection Drift Migration Fluctuation or deviation

11 1 Hardy -Weinberg Mendel A. B. Simpson C. 11

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