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The Rise and Fall of Panselectionism Michael R. Dietrich Department of Biological Sciences Dartmouth College

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1 The Rise and Fall of Panselectionism Michael R. Dietrich Department of Biological Sciences Dartmouth College

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3 “Once upon a time, the world seemed simple when viewed through the eyes of evolutionary biologists. All genomes were tightly controlled by various forms of natural selection. … This idyllic world began to crumble in 1968, when Kimura made his modest proposal that most allele substitutions and polymorphisms do not substantially affect an organism’s fitness and are governed, not by positive or balancing selection, but by random drift.” Alexey Kondrashov,“Fruitfly Genome is not Junk,” Nature 437 (October 2005) 1106.

4 Motoo Kimura 1968 “Evolutionary Rate at the Molecular Level,” Nature 217: Cost of Selection

5 Varieties of Evidence in Support of the Neutral Theory Kimura (1968a)King and Jukes (1969)cost of selection Kimura (1968b)molecular clocksynonymous mutation differences in rates of change for amino acid and DNA sequences amino acid composition distribution of conserved and nonconserved regions in different proteins

6 The Neutralist-Selectionist Controversy Begins The Non-Darwinian Challenge Kimura (1968a) King and Jukes (1969) The Darwinians Respond Richmond (1970) Clarke (1970) Between Boston and Berkeley 1970 Boston Meeting 1971 Berkeley Meeting

7 The Neutralist/Selectionist Controversy 3 in 1 Interpretation (1)The Molecular - Morphological Split

8 The Neutralist/Selectionist Controversy 3 in 1 Interpretation (1)The Molecular - Morphological Split (2) Neutrality and Selection at Protein Level late 1980s

9 The Neutralist/Selectionist Controversy 3 in 1 Interpretation (1)The Molecular - Morphological Split (2) Neutrality and Selection at Protein Level late 1980s (3) Neutrality and Selection at DNA Level Present (?)

10 The Molecular Clock E. Zuckerkandl and L. Pauling (1962, 1965) Rate of amino acid substitution is approximately proportional to time

11 From R. E. Dickerson, “The Structure of Cytochrome c and the Rates of Molecular Evolution,” Journal of Molecular Evolution 1 (1971)

12 The Molecular/Morphological Split Beginning in 1962, the molecular clock contributed to a split between evolution at the Organismal or Morphological Level and evolution at the Molecular Level. 1964G. G. Simpson argued against the idea that molecules "have evolved by some sort of internal constant-rate mutational process and not in an irregular adaptive way." 1965 Emile Zuckerkandl and Linus Pauling acknowledge the growing tension between "organismal evolutionists and taxonomists" and "pure (very unorganismal) biochemists.” "According to them [the biochemists] (and to us), what most counts in the life sciences today is the uncovering of the molecular mechanisms that underlay the observations of classical biology."

13 Gears for the Clock Zuckerkandl and Pauling invoked both selection and drift to explain the mechanism of the clock After 1968Motoo Kimura, Allan Wilson and others used the neutral theory of molecular evolution to explain the mechanism of the clock, because the rate of substitution for neutral mutants is the same as the mutation rate.

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15 The Power of Paradox The molecular/morphological paradox was used to negotiate a place for molecular evolution within evolutionary biology. It was invoked during a time of increasing division between organismal and molecular biology. It was always offered with a resolution. It allowed molecular evolution to be understood as distinct and interesting in its own right, but compatible with evolution at the organismal level.

16 Dividing the Domain of Evolution Decoupling the molecular and organismal levels as a means of controversy closure. Explanation for divergent rates and the existence of the molecular clock

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18 The Persistence of the Neutralist-Selectionist Controversy By mid-1970s No longer a molecular/morphological conflict At the molecular level (Protein and DNA) Problem of explaining polymorphism Problem of rate constancy

19 The Neutralist/Selectionist Controversy For both Protein and DNA disputes Relative Frequency Controversy Proportion (relative importance) of neutral mutations Prevalence (relative importance) of random drift Always a selection-drift mix

20 Controversy Dynamics Polarization and Depolarization

21 NeutralistsSelectionists “Non-Darwinians”“Naïve Pan-selectionists” LEVELS MolecularOrganismal Drift and selectionSelection Pluralist ApproachUnified Approach The Neutralist/Selectionist Controversy

22 Old Drifters Never Die Theodosius Dobzhansky Architect of the Modern Synthesis

23 Theodosius Dobzhansky to Jack King. June 8, 1970

24 Theodosius Dobzhansky to Jack King. June 8, 1970

25 Theodosius Dobzhansky to Jack King. June 8, 1970

26 Testing Neutrality 1971 Sixth Berkeley Symposium on Mathematical Statistics and Probability Motoo Kimura and Tomoko Ohta “A principle virtue of the neutral theory is that it generates testable predictions and in so doing promises to "emancipate" biologists from "naive panselectionism”.” G. L. Stebbins and R. C. Lewontin The neutral theory is ""empirically void" because it has no set of potential falsifiers."

27 The Trouble with Testing DateAuthorsDesigned to Detect 1972Warren EwensDistribution of allele frequencies; actual and effective numbers of alleles No Statistical Power 1973R. C. Lewontin & J. Krakauer Heterogeneity among loci as a test of selection 1974Francisco Ayala, et al.Distribution of heterozygous loci Excess of rare alleles T. Yamazaki & T. Maruyama Relationship between gene frequency and heterozygosity; actual and effective numbers of alleles M. Nei, P. Fuerst & P. Chakaraborty Gene frequency and heterozygosity

28 “In Defense of Naive Pan-selectionism” “virtually any change in amino acid composition of any protein molecule produces a molecule of slightly different properties and therefore of slightly different selective value from the original.” (p. 23) Christopher Wills, “In Defense of Naïve Pan-selectionism,” The American Naturalist 107 (1973)

29 “Naive Pan-selectionism” Christopher Wills, “In Defense of Naïve Pan-selectionism,” The American Naturalist 107 (1973)

30 Was there a panselectionist orthodoxy in the 1960s? “Naïve pan-selectionism” was reified by an extremely polarized controversy. Most biologists acknowledged a minor role for drift.

31 From Proteins to DNA 1983 Martin Kreitman Sequences ADH genes in Drosophila

32 From Proteins to DNA M. Kreitman and M. Aguade, “Excess Polymorphism at the ADH locus in Drosophila melanogaster,” Genetics 114 (1986)

33 Neutrality Tests Date and NameAuthorsDesigned to Detect 1987 HKAHudson, Kreitman, and Aguade Differences in variation levels not accountable by constraints 1989 Tajima’s DTajimaSkew in frequency distribution 1991 McDonald Kreitman McDonald and Kreitman Adaptive evolution 1994 HudsonHudson, Bailey, Skarecky, Kwiatowski, and Ayala Unexpected low variation within an allele class 1996 Fu W and others FuDepartures in frequency distribution related to population subdivision and growth 1999 Wall B and Q WallLinkage disequilibrium between adjacent segregating sites

34 Neutrality Tests

35 James Crow Neutral Theory Provides a Null Model 1964 Instrumental Use Post-1985 Empirical Use Assume neutrality until disproven by a statistical test (Neutral Models in Biology. Matthew H. Nitecki and Antoni Hoffman, Eds., Oxford University Press 1987.)

36 Pluralism and Panselection To what extent did the neutral theory contribute to the decline of panselectionism? In what sense did this render evolutionary biology more pluralistic?

37 The Problem with Panselectionism “Three Kinds of Adaptationism”  Empirical: “Natural selection is a powerful and ubiquitous force, and there are few constraints, except general and obvious ones, on the biological variation that fuels it.”  Methodological: “The best way for scientists to approach biological systems is to look for features of adaptation and good design.”  Explanatory: Explaining “the apparent design of organisms, and the relations of adaptedness between organisms and their environments” is “the core intellectual mission of evolutionary theory.” Peter Godfrey Smith, “Three Kinds of Adaptationism,” in Adaptationism and Optimality. S. Hecht and E. Sober, Eds. Cambridge University Press, 2001,

38 The Problem with Panselectionism Three Kinds of Panselectionism  Empirical: “Natural selection is a powerful and ubiquitous force, and there are few constraints, except general and obvious ones, on the biological variation that fuels it.”  Methodological: “The best way for scientists to approach biological systems is to look for evidence of natural selection in some form.”  Explanatory: Explaining the effects of selection is “the core intellectual mission of evolutionary theory.” Peter Godfrey Smith, “Three Kinds of Adaptationism,” in Adaptationism and Optimality. S. Hecht and E. Sober, Eds. Cambridge University Press, 2001,

39 The Problem with Panselectionism Empirical Panselectionism Extreme formulation (All selection, all the time) Rejected or Never Held? Importance of Relative Frequency Issue Varies depending on level and age

40 The Problem with Panselectionism Methodological Panselectionism Attacked by Gould and Lewontin (1979) Defended by Mayr (1983) Best method available Drift cannot be detected Overturned at molecular level by post neutrality tests

41 The Problem with Panselectionism Explanatory Panselectionism Richard Dawkins’ “Universal Darwinism” Can the neutral theory be ignored? Struggle for Authority Should the molecular and organismal levels be integrated?

42 Molecular-Morphological Integration HSP 90 A Neutral Evolutionary Capacitor Suzanne Rutherford and Susan Linquist, “HSP90 as a capacitor for morphological evolution,” Nature 396 (1998),


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