The organismic critique within
the Modern Synthesis and after.
Philippe Huneman
IHPST, Paris
Questions about the Modern Synthesis
(MS)
- Is It over ? Has it been replaced ? Should it be
over / extended ?
But also :
- Did it really exist as a synthesis (i.e., as a
unity)?
- What was the nature of such unity (theory,
set of models, etc.)
My 2 independent projects
1. Understand the relations between the
emerging philosophy of biology (in the 60s)
and the Modern Synthesis
(role of Mayr in setting the debates : autonomy claims,
reductionnism, evolutionism-centered view, etc.)
2. Assess the current critique of the MS from the
view point of the organisms
-> today : what about the MS on this issue?
The space of controversies
Genes
Mostly natural selection ( adaptationnism)
• Dawkins
Dawkins
• Lyn
Genes
Not only natural selection (no adaptationnism)
Organisms
Mostly natural selection
( adaptationnism)
Mayr
Lynch
Michod
Mayr
Organisms
• Gould
Not only
natural selection (no adptationnism)
Gould
The space of controversies
Genes
Mostly natural selection ( adaptationnism)
• Dawkins
Dawkins
Optimisation line
• Lyn
Organisms
Mostly natural selection
( adaptationnism)
Mayr
Genes
Not only natural selection (no adaptationnism)
Mayr
•
Lynch
Michod
Organisms
Not only natural selection (no
Gould
adaptationnism)
Gould
Organismic
line
• Question : what does it owe to the « Modern
Synthesis » (as a not necessarily synthetic set
of books, papers, etc.?)
• Outline
– Evolutionary organicism, then and now
– Population genetics and the Modern Synthese(s)
I.
EVOLUTIONARY ORGANICISM,
THEN AND NOW ?
A 2 decades-long critique of
suborganismic/adaptationist biology
- Gould (1983): the « hardening of the
Synthesis »
- Walsh (2010) The triumph of « suborganismal
biology » (= MS) and the recent prospects for
« organismal » biology (phenotypic plasticity,
adaptivity of organisms)
What is crucial : the status of adaptation.
(Depew 2010, on the duality (UK /US) of the Synthesis;
the « hardening » is the triumph of the former)
Received view : an adaptation = a (trait) result(ing) from
natural selection
Challenges : adaptation as changing the environment
(Odling-Smee et al. 2003); adaptation as adaptive
plasticity (Walsh 2003, 2010, West-Eberhardt...)
Old problem : how to get the adaptedness of organisms ?
The current organismic critique of MS,
fourfold
(after Huneman HPLS 2010)
Niche construction
Newman and Muller Evo-devo
Bauplan
?
WestEberhardt,
adaptive
plasticity
But: organismic critique is not new
Indeed it was a crucial moment in the
consolidation/ aftermath of the MS:
Ernst Mayr, “Where Are We?” Cold Spring Harbor Symposium on Quantitative
Biology 24 (1959): 1–14.
Ernst Mayr, “Cause and Effect in Biology” Science 134 (1961): 1501–06;
Theodosius Dobzhansky, “Biology, Molecular and Organismic,” American Zoologist
4 (1964): 443–52.
Sewall Wright, “Gene and Organism,” The American Naturalist 87, no. 832 (1953):
5–18.
George Gaylord Simpson, “The Status of the Study of Organisms,” American
Scientist 50, (1962): 36–45.
case of Waddington left aside here
Is this a last stage of the MS ? A first round of interpretation ?
Organicism, 60s.
• The level of organicism is emphasized as
proper to biology
• Especially against the rise of Molecular
Biology
Arguments by Wright (levels) and Mayr (2
causes) were crucially influential …
Essential idea, 1.
• Biology is hierarchised.
Reduction, in Nagel’s
sense (Dobzhansky,
Mayr cite Nagel 1961)
does not work.
Each level is not deducible
from the precedings
Wright, 1953
Mayr 1955
• Critique of « beanbag genetics »
One- or two-loci model are unable to capture the
complexity of causal interactions in evolutionary
dynamics
Evolutionary thinking is holistic and
interactionist - Dobzhansky
• “Talking about traits as though they were independent
entities is responsible for much confusion in biological
and especially in evolutionary thought” (1970, 65).
• “A change in the genotype alters the reaction norm,
and some of the alterations may enable the new
genotype to produce a harmonious response where
the ancestral has been a failure … Selection deals not
with the genotype as such, but with its dynamic
properties, its reaction norm, which is the sole
criterion of fitness in the struggle for existence.” (1937,
170).
Essential idea, 2. (Mayr).
• What’s proper to biology is
evolutionary style
explanations. (« ultimate »)
• « Nothing in biology makes
sense etc. » (Dobzhansky
1964.)
The strategy.
(1) + (2) = the proper biological (= evolutionary)
level is organism (and beyond).
MAYR
Notice : curiously, evolutionary
explanation and organicism are tied
(whereas, one could think that
evolutionary explanations are levelindependent)
•
•
A first reason : genes are too close
to chemistry (via molecular biology)
A second reason : critique of
genetic atomism (as misleading
abstraction); interactionism:
concrete complexity occurs at the
organismic level
In biology, a second kind of
explanation may be added to the
first, or reductionist explanation,
made in terms of physical,
chemical and mechanical
principles. This second form of
explanation, which can be called
compositionist in contrast to
reductionist, is in terms of
adaptive usefulness of structures
and processes to the whole
organism and to the species of
which it is a part, and still further,
in terms of ecological function in
which the species occurs.
(Simpson 1964)
II.2.
MAYR’S ORGANICISM
Mayr ?
“It is hard to exaggerate the significance of Mayr's
defense of the proximate/ultimate distinction in
establishing philosophy of biology as a legitimate
special area of inquiry”
(Beatty 1994)
Most quoted author in Hull’s classical « What
philosophy of biology is not ? » (19 occurrences)
Critique of genetic atomism
Two polemic stances:
1942-53, downplay the role of geneticists in the
founding of modern evolutionary biology
1955-later (after the discovery of DNA): vindicate
the specificity of evolutionary biology against
molecular biology
Historical sketch of MS by Mayr
« Several historians have mistakenly thought that this synthesis within genetics had solved
all the problems of Darwinism. That assumption, however, failed to take account of an
important gap. One of the two major branches of evolutionary biology, the study of the
origin of biodiversity, had been left out of the major treatises of Fisher, Haldane, and
Wright. Actually, unknown to these geneticists, the problems of the origin of biodiversity
had already been solved in the 1920s by several European naturalists, most important
among them, Moritz Wagner, Karl Jordan, Poulton, Chetverikov and Stresemann. Thus,
evolutionary biology around 1930 found itself in a curious position. It faced two major
seemingly unsolved problems: the adaptive changes of populations and
the origin of biodiversity. Two large and very active groups of evolutionists worked
on these problems. One of these groups consisted of the population geneticists. As
summarized in the works of Fisher, Haldane, and Wright, this group had solved the
problem of gradual evolution of populations through natural selection. But they had
not made any contribution to the problem of how species arise (speciation) - that is, to
the problem of the origin of biodiversity. The other group of evolutionists consisted of
the naturalists taxonomists.”
• The two explananda of evolution : adaptation,
diversity
(notice how it differs from Dobzhansky, quoted above)
About Systematics and the origins of species (1942): “The real
objective of my volume was to explain a whole set of
phenomena,—such as species and speciation, as the effects of
selection on populations, as the role of geography at the level of
species and populations, and as the role of species in
macroevolution,— that were omitted in the accounts of the
geneticists or that were based on the findings of the systematists,
such as in the volumes of Dobzhansky, Timoféeff-Ressovsky and
Huxley”
“It is now understood that evolution consists in two major processes,
the changes (usually adaptational) of populations in time, and the
multiplication of species in space that is the origin of new organic
diversity. The latter process, more often called speciation, has been
clouded with confusion ever since 1859. Darwin in his early
unpublished writings (1837 to 1844) had come to the conclusion
that geographic isolation was a necessary prerequisite for
speciation and that therefore allopatric speciation was the
prevailing, if not the only, form of speciation (Kottler 1978; Sulloway
1979). However, by 1859 when he published the Origin, Darwin had
concluded that sympatric speciation, the splitting of a single
population without geographic isolation, was at least equally
common.”
Mayr, JHB paper on Weissmann, 1985
What’s the trouble with population
genetics ??
Speciation appears when genetic environment of
the genes change (e.g. at boundaries of
territories). (« Change of environment and speciation » (1954))
• This assumes that the effect of genes is
(organsims- and gene-contextual) dependent.
• Usual PG models (atomistic etc.) are not realistic
• What causally accounts for speciation are
changes in reproductive barriers which imply
whole genotypes and organismic behaviour
Consequences
« Population » is not exemplarily represented by
population genetics !
A population is indeed biological : it reproduces itself through
the reproduction of some organisms.
« In the study of biological species one deals with biological populations. (…)
Only a small fraction of any biological population reproduces, because not
every individual in a population survives up to the reproductive age and
reproduces successfully. This is true on the average of only two of the
total number of a prenatal pair in a sexually reproducting species. »
(« What is a species and what it is not », Phil Sci 1996)
From the viewpoint of diversity questions, the causal consistency
of population is due to organisms (and not genes)
Consequences, 2
-> Population genetics does not exemplify the
evolutionary style of explanation:
“Evolutionary biology dealing with highly complex
systems [not genes, PH] operated by historically
evolved genetic programs, must pursue a very different
strategy of research in order to provide explanations.
Its most productive method is the comparative
method, for which the taxonomists have laid the
foundation. Indeed I can hardly think of a evolutionary
problem that has not developed out of some findings of
taxonomy.” (“the role of systematics in biology”)
• Hence Mayr rejects the
textbook definition of
evolution as « changes in
allele frequencies in a
population ».
– “Evolution is not a change in
gene frequencies, as is claimed
so often, but the maintenance
(or improvement) of
adaptedness and the origin of
diversity. Changes in gene
frequency are a result of such
evolution, not its cause.” (Mayr
1997, 2093).
• Mayr would subscribe to
Walsh’s idea that it
providses only a shadow
(« pseudo-process » sensu
Salmon) of the evolutionary
process.
• This is not at all the MS
targeted by Walsh,
Muller, Gerhardts and
Kirschner, WestEberhardt etc.
• Defining a version of MS
-> role of population
genetics (viz. the
result/cause diff.).
II. (the speculative part…)
II. POPULATION GENETICS AND THE
VERSIONS OF MODERN SYNTHESIS
• Claim 1, weak. Population genetics is central in
evolutionary biology because it mathematically
explains why evolution by NS is possible (eg
Gayon 1998) (assuming particular inheritance)
• Claim 2, strong. Population genetics provides the
fine-grained knowledge of the process of
evolution as a population level phenomenon
(Hamilton, Maynard-Smith, Williams, Price, Grafen, Michael Lynch,
etc.)
The call for an extended MS often rejects 2.
Especially : « PG is not a causal knowledge of
evolution. »
The issue : is PG a statistical or a causal
understanding of evolutionary dynamics ??
A parallel in quantitative genetics
• Lande-Arnold 1983,
measurement of selection
on correlated characters
(i=1….n)
• G = variance-covariance
matrix of breeding values
• P-1 s = set of partial
regression of relative
fitnesses on characters
(Corresponds to univariate
breeder’s equation R=hs)
• Major idea: G represents how the genic
architecure constrains the response to
selection
• Yet major problems to get causal explanations
out of it (Pigliucci 2005; Barton and Turelli
1989).
Back: Two views of PG
statistical
• Abstract away from causes
in general
• The content is pure maths
(Price equ.) and statistics
• Hence causes have to be
plugged in from the outside
• They are the causes of
fitness (pertaining to
ecology, physiology, etc.)
• It is not the core of MS but
has instrumental value
/
causal
• What causes evolution is
differential replication,
which is the explanandum
of PG
• Hence PG captures the
process of Natural Selection
• Therefore it is the core of
evolutionary theory
• And e.g. grounds its
methodology (FTNS ->
optimisation methods).
Fisher’s take on PG.
The statement of the principle of Natural Selection in the form of a theorem
determining the rate of progress of a species in fitness to survive (this
term being used for a well-defined statistical attribute of the population),
together with the relation between this rate of progress and its standard
error, puts us in a position to judge of the validity of the objection which
has been made, that the principle of Natural Selection depends on a
succession of favourable chances. The objection is more in the nature of
an innuendo than of a criticism, for it depends for its force upon the
ambiguity of the word chance, in its popular uses. The income derived
from a Casino by its proprietor may, in one sense, be said to depend upon
a succession of favourable chances, although the phrase contains a
suggestion of improbability more appropriate to the hopes of the patrons
of his establishment. It is easy without any very profound logical analysis
to perceive the difference between a succession of favourable deviations
from the laws of chance, and on the other hand, the continuous and
cumulative action of these laws. It is on the latter that the principle of
Natural Selection relies. (Fisher GTNS, 1930, 37.)
A sketch of a possible causal argument.
Fisher’s parallel with statistical mechanics : FTNS and 2nd law as
two main causal laws
StatMech is a causal
knowledge, even if
statistically abstracting
from many causal
interactions, because it
averages away too-finegrained causes
PG is possible because
many interactions
between genes in the
genetic background of
one or two loci in a
population can be
averaged out, and by
tracing the dynamics of
the focal loci one
captures its dynamics
on any background
Note : About adaptationism
• PG as such is neutral about adaptationism –
nothing entails that NS is the most important
cause of evolution
• How to derive this darwinian claim ?
• Only if the fundamental theorem of NS is true
• Fisher’s position : PG is a causal knowledge of
evolution, FTNS grounds adaptationism
• FTNS (Frank &Slatkin 1992) is about the change in
mean fitness caused directly by NS, hence
assumes a causal understanding of population
dynamics.
Two rhetorics of natural selection
Hull
• Differential replication
of replicators according
to interactions of
interactors
“Interactors” is the level
where causation is
Dawkins
• Differential replication
of replicators
embedded in vehicles
(Differential) “replication”
is where causation
takes place
A by-product of this alternative
Debates on gene selectionism:
Classical counter-argument (Sober 1982): gene
selection is bookkeeping, does not capture
causal processes.
(whereas gene selectionists would say that causal
dispositions are in the relatedness value r, e.g.
West et al. 2007)
Conclusion
At least two versions of MS
MS M : organicism; PG not the central core
MS F : PG = science of the process of ENS; core of
the evolutionary theory (Lynch’s dictum)
(may be analogous to Depew’s distinction, UK and US
styles in MS…)
The space of controversies
Genes
Mostly natural selection ( adaptationnism)
• Dawkins
Dawkins
• Lyn
MS F
Genes
Not only natural selection (no adaptationnism)
Organisms
Mostly natural selection
( adaptationnism)
Mayr
Lynch
Michod
Mayr
MS M
Organisms
• Gould
Not only
natural selection (no adptationnism)
Gould
a. Calls for « organismal » biology target MS F
Issues about the causal nature of PG seem
unavoidable.
b. In terms of interpreting the models (especially
PG) MS is NOT a synthetic theory
c. Extending (resp. expanding, overcoming, etc.)
the Modern Synthesis can’t make sense
except if one specifies which Synthesis.