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The Rise and Fall of
Panselectionism
Michael R. Dietrich
Department of Biological Sciences
Dartmouth College
[email protected]
http://hrst.mit.edu/hrs/evolution/public/anyside0.html
“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.
Motoo Kimura
1968 “Evolutionary Rate at the
Molecular Level,” Nature 217:
624-626.
Cost of Selection
Varieties of Evidence in Support of the
Neutral Theory
Kimura (1968a)
King and Jukes (1969)
cost of selection
cost of selection
Kimura (1968b)
molecular clock
synonymous mutation
synonymous mutation
differences in rates of change
for amino acid and DNA
sequences
amino acid composition
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distribution of conserved and
nonconserved regions in different
proteins
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
The Neutralist/Selectionist Controversy
3 in 1 Interpretation
(1)The Molecular - Morphological Split
1962 - 1972
The Neutralist/Selectionist Controversy
3 in 1 Interpretation
(1)The Molecular - Morphological Split
1962 - 1972
(2) Neutrality and Selection at Protein Level
1968 - late 1980s
The Neutralist/Selectionist Controversy
3 in 1 Interpretation
(1)The Molecular - Morphological Split
1962 - 1972
(2) Neutrality and Selection at Protein Level
1968 - late 1980s
(3) Neutrality and Selection at DNA Level
1985 - Present (?)
The Molecular Clock
E. Zuckerkandl and L. Pauling (1962, 1965)
Rate of amino acid substitution is approximately
proportional to time
From R. E. Dickerson, “The Structure of Cytochrome c and the Rates of Molecular Evolution,” Journal
of Molecular Evolution 1 (1971) 26-45.
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.
1964 G. 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."
Gears for the Clock
1962-1967 Zuckerkandl and Pauling invoked both
selection and drift to explain the mechanism of the
clock
After 1968 Motoo 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.
The Molecular/Morphological
Paradox
"Molecular evolution proceeds in a
rather regular fashion with respect to
time. By contrast, organismal evolution
is classically considered to be an
irregular process, some species (e.g.,
placental mammals) changing rapidly,
while others (e.g., frogs) change slowly.
The paradox may be resolved by
postulating the random fixation of
mutations producing amino-acid
substitutions that have no effect,
favorable or unfavorable, on protein
function and hence no effect on
anatomy, physiology or behavior."
Allan Wilson (1971)
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.
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
Levels
Molecular
v.
Evolutionary
Biology
Systematics
Evolution
Neither
morphological
nor molecular
traits are better
for systematics.
Natural Selection
acts only on the
organismal level.
The organismal
level has causal
and explanatory
primacy.
Compatiblist
Compatiblist
Anti-reductionist
Experimental
biology is
molecular
biology.
Molecular traits
are better for
systematics.
Natural Selection
acts only on the
organismal level.
Random genetic
drift is the most
important causal
factor at the
molecular level.
Argument from
Human Values.
Organismal
Molecular
Argument from
Ultimate /
Proximate
Distinction.
Molecular biology
is foundational.
Reductionist
Reductionist
Compatiblist
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
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
Controversy Dynamics
Polarization and Depolarization
The Neutralist/Selectionist Controversy
Neutralists
Selectionists
“Non-Darwinians”
“Naïve Pan-selectionists”
LEVELS
Molecular
Organismal
Drift and selection
Pluralist Approach
Selection
Unified Approach
Old Drifters
Never Die
Theodosius
Dobzhansky
Architect of
the Modern
Synthesis
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Theodosius
Dobzhansky to
Jack King.
June 8, 1970
Theodosius
Dobzhansky to
Jack King.
June 8, 1970
Theodosius
Dobzhansky to
Jack King.
June 8, 1970
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."
The Trouble with Testing
Date
Authors
Designed to Detect
1972
Warren Ewens
Distribution of allele frequencies;
actual and effective numbers of
alleles
No Statistical Power
1973
R. C. Lewontin & J.
Krakauer
Heterogeneity among loci as a test
of selection
1974
Francisco Ayala, et al.
Distribution of heterozygous loci
Excess of rare alleles
1972-74
T. Yamazaki & T.
Maruyama
Relationship between gene
frequency and heterozygosity; actual
and effective numbers of alleles
1976-78
M. Nei, P. Fuerst &
P. Chakaraborty
Gene frequency and heterozygosity
“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) 23-34.
“Naive Pan-selectionism”
Christopher Wills, “In Defense of Naïve Pan-selectionism,” The American Naturalist 107 (1973) 23-34.
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.
From Proteins to DNA
1983 Martin Kreitman
Sequences ADH genes in
Drosophila
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From Proteins to DNA
KREITM AN: We wanted to know if there was hidden variation at the protein level. And
we did not find any. In fact, we did find a lot of variation, but it stood as a very powerful
contrast in a way. Because it wasnΥt just that there was no variation. There was lots of
variation; it wasnΥt at the replacement sites. And that confirmed in some sense what we
already know. ThatΥs why I played it down. That there are selective constraint and that
was really the predomi nant forces.
M. Kreitman and M. Aguade, “Excess Polymorphism at the ADH locus in Drosophila melanogaster,”
Genetics 114 (1986) 93-110.
Neutrality Tests
Date and Name
Authors
Designed to Detect
1987 HKA
Hudson,
Kreitman, and
Aguade
Differences in variation levels not
accountable by constraints
1989 Tajima’s D
Tajima
Skew in frequency distribution
1991
McDonald
Kreitman
McDonald and
Kreitman
Adaptive evolution
1994 Hudson
Hudson, Bailey, Unexpected low variation within an
Skarecky,
allele class
Kwiatowski,
and Ayala
1996 Fu W
and others
Fu
Departures in frequency distribution
related to population subdivision and
growth
1999
Wall B and Q
Wall
Linkage disequilibrium between
adjacent segregating sites
Neutrality Tests
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.)
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?
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, 335-357.
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, 335-357.
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
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 post1985 neutrality tests
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?
Molecular-Morphological Integration
HSP 90
A Neutral
Evolutionary
Capacitor
Suzanne Rutherford and Susan
Linquist, “HSP90 as a capacitor for
morphological evolution,” Nature 396
(1998), 336-342.