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21 Coffroth, M.A. and Lasker, H.R. (1998) Larval
paternity and male reproductive success of a
broadcast-spawning gorgonian, Plexaura
kuna, Mar. Biol. 131, 329–337
22 Willis, B.L. et al. (1997) Experimental
hybridization and breeding incompatibilities
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23 Heyward, A.J. and Babcock, R.C. (1986) Selfand cross-fertilization in scleractinian corals,
Mar. Biol. 90, 191–195
24 Miller, K.J. and Babcock, R.C. (1997)
Conflicting morphological and reproductive
species boundaries in the coral genus
Platygrya, Biol. Bull. 192, 98–110
25 Szmant, A.M. et al. (1997) Hybridization within
the species complex of scleractinian coral
Montastraea annularis, Mar. Biol. 129, 561–572
26 Stoddart, J.A., Babcock, R.C. and Heyward, A.J.
(1988) Self-fertilization and maternal enzymes
in the planulae of the coral Goniastrea
favulus, Mar. Biol. 99, 489–494
27 Ayre, D.J. and Resing, J.M. (1986) Sexual and
asexual production of planlulae in reef corals,
Mar. Biol. 90, 187–190
28 Benzie, J.A.H., Haskell, A. and Lehman, H.
(1995) Variation in the genetic composition of
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palifera) populations from different reef
habitats, Mar. Biol. 121, 731–739
Fisher, R.A. (1941) Average excess and average
effect of a gene substitution, Ann. Eugen. 11, 53–63
Lande, R. and Shemske, D.W. (1985) The
evolution of self-fertilization and inbreeding
depression in plants. I. Genetic models,
Evolution 39, 533–544
Harder, L.D. and Wilson, W.G. (1998) A
clarification of pollen discounting and its
joint effects with inbreeding depression on
mating system evolution, Am. Nat. 152, 684–695
Szmant-Foelich, A., Reutter, M. and Riggs, L.
(1985) Sexual reproduction of Favia fragum
(Esper): lunar patterns of gametogenesis,
embryogenesis and planulation in Puerto
Rico, Bull. Mar. Sci. 37, 880–892
Hall, V.R. and Hughes, T.P. (1996)
Reproductive strategies of modular organisms
– comparative studies of reef-building corals,
Ecology 77, 950–963
Waller, D.M. (1993) The statics and dynamics
of mating system evolution, in The Natural
History of Inbreeding and Outbreeding
(Thornhill, N., ed.), pp. 97–117, University of
Chicago Press
Uyenoyama, M.K. (1986) Inbreeding and the
cost of meiosis: the evolution of selfing in
The modern synthesis, Ronald Fisher
and creationism
The ‘modern evolutionary synthesis’ convinced most biologists that natural selection
was the only directive influence on adaptive evolution. Today, however,
dissatisfaction with the synthesis is widespread, and creationists and antidarwinians
are multiplying. The central problem with the synthesis is its failure to show (or to
provide distinct signs) that natural selection of random mutations could account for
observed levels of adaptation.
Egbert Leigh, Jr is at the Smithsonian Tropical Research Institute, Smithsonian Institution,
Washington, DC 20560-0580, USA.
T
TREE vol. 14, no. 12 December 1999
37
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synthesis untestable8, sterile9,10 and outmoded11: creationists and antidarwinians
(Box 1) are as numerous and as vocal
as ever.
Making natural selection a
deus ex machina
Egbert Giles Leigh, Jr
he modern evolutionary synthesis1 is
founded upon the proposition that
natural selection is the directive influence on adaptive evolution. This synthesis was established by combining deductive reasoning with the elimination of
competing hypotheses by empirical research. Work of systematists2 and geneticists3,4, on the stages of speciation, confirmed Darwin’s view that speciation
rarely involves discontinuous ‘saltations’
(polyploidy being the principal exception). Geneticists3–5 falsified neo-Lamarckism and mutation-driven theories of
evolution; and paleontologists6 revealed
36
populations practicing partial biparental
inbreeding, Evolution 40, 388–404
Uyenoyama, M.K. and Antonovics, J. (1987) The
evolutionary dynamics of mixed mating
systems: on the adaptive value of selfing and
biparental inbreeding, in Perpectives in
Ethology, Vol. 7: Alternatives (Bateson, P.P.G.
and Klopfer, H., eds), pp. 125–152, Plenum Press
Ayre, D.J. and Dufty, S. (1994) Evidence for
restricted gene flow in the viviporous
coral Seriatophora hystrix on Australia’s
Great Barrier Reef, Evolution 48, 1183–1201
Ayre, D.J., Hughes, T.P. and Standish, R.J.
(1997) Genetic differentiation, reproductive
mode, and gene flow in the brooding coral
Pocillopora damicornis along the Great
Barrier Reef, Australia, Mar. Ecol. Prog. Ser. 59,
175–187
Yu, J.K. et al. (1999) Genetic structure of a
scleractinian coral, Mycedium elephantotus,
in Tawain, Mar. Biol. 133, 21–28
Grosberg, R.K., Levitan, D.R. and Cameron, B.B.
(1996) Characterization of genetic structure
and genealogies using RAPD-PCR markers: a
random primer for the novice and nervous, in
Molecular Zoology: Advances, Strategies, and
Protocols (Ferraris, J.D. and Palumbi, S.R., eds),
pp. 67–100, Wiley Liss
the environmental, opportunity-driven
context of evolution, applying the ‘coup
de grace’ to theories of mutation-driven
orthogenesis. Eliminating these pseudoexplanations seemed to lift a thick fog
from the subject. Mayr7 remarked, ‘No
one who has not witnessed it himself can
imagine the confusion and dissension
that characterized the pre-Synthesis
period.’ The three classics2,4,6 that established the American version of the synthesis overflow with a sense of triumph
and hope: finally there was a reliable
basis for understanding evolution. However, biologists have since declared the
The primary problem with the synthesis is that its makers established natural selection as the director of adaptive
evolution by eliminating competing
explanations7, not by providing evidence
that natural selection among ‘random’
mutations could, or did, account for observed adaptation (Box 2). Mayr12 remarked, ‘As these non-Darwinian explanations were refuted during the synthesis
… natural selection automatically
became the universal explanation of evolutionary change (together with chance
factors).’ Depriving the synthesis of plausible alternatives, which seemed such a triumph, in fact sowed the seeds of its faults.
Direct demonstration of the relationships between available variation, natural selection and evolution was neglected
for several reasons. First, the task seemed
formidable13. The physicist Polkinghorne
observed:
‘Someone like Richard Dawkins can
present persuasive pictures of how the
sifting and accumulation of small differences can produce large-scale developments, but, instinctively, a physical scientist would like to see an estimate,
however rough, of how many small steps
Published by Elsevier Science Ltd. PII: S0169-5347(99)01725-5
495
PERSPECTIVES
Box 1. Definitions
Creationists are those who believe that God created the universe, and all species alive today, in a geological instant several thousand years ago. The usual motive for creationism is conformity to a literal
interpretation of the Book of Genesis or some analogous scripture.
Antidarwinians are those who accept the great age of the universe and the fact of evolution as manifest
in the evidence for common ancestry of all living things, but reject natural selection of ‘random’
mutations as an adequate cause of adaptive evolution. Antidarwinism might have a scientific or a
religious basis.
‘Random’ mutations are mutations whose effects (however, not necessarily their rate of occurrence) are
unrelated to the needs of the organisms affected.
Box 2. How can one ‘prove’ the synthesis?
How can someone not committed to mechanistic explanations of evolution be convinced that natural
selection of random mutations drives adaptive evolution? This problem is not easy. We cannot ‘postdict’
adaptive radiations in the same way that physicists predict movement of planets, development of stars
or even (perhaps) the universe’s first three minutes14. The synthesis is testable, but its tests have produced
no verification as triumphant as the precise analogy between an apple’s fall and the motion of Mars21.
Fisher tried to prove the synthesis by showing that: random mutations can produce favorable variation,
as indicated by his ‘mutation model’; favorable mutations occur frequently, as evidenced by sexual
reproduction; and natural selection spreads even slightly favorable mutations, as demonstrated by his
theory of dominance.
Others analyse specific examples of diversification or adaptation to see if the synthesis can explain
them10. Some study speciation in enough detail to show how, and by what stages, natural selection of
available variation caused the process39,40. Others analyse specific adaptive breakthroughs to show the
genes involved, the precise molecular mechanisms of their effects and why selection favored each one41.
Leigh tried to identify circumstances indicating the crucial role of natural selection in selected major
transitions of evolution34. Finally, one can show in what respect living things are organized to facilitate
natural selection on their populations26,36.
Box 3. Modelling ‘random’ mutation
Fisher5 imagined a locus affecting a characteristic whose state can be represented by a point in an ndimensional space. Let its actual state in some organism be A, let its optimum be O, and let A’s deviation
from the optimum decrease the bearer’s fitness proportionally to the square |A2O|2 of the Euclidean distance between A and O. Let a random mutation of magnitude |r| in A create a new state A1r, located randomly on the surface of the sphere of radius |r| about A. The mutation is favorable if |A1r2O|2,|A2O|2.
The probability that the mutation is favorable increases as |r| decreases, and is 1/2 for infinitesimal |r|.
For a fixed value of |r|/|A2O|, the probability that the mutation is favorable is larger the lower n becomes.
This model seems incredibly simplistic. Nonetheless, Orr42 used this model to successfully predict
the distribution of relative contributions of different genes affecting the difference between related
populations in a quantitative characteristic.
take us from a slightly light-sensitive cell
to a fully formed insect eye, and of approximately the number of generations required for the necessary mutations to
occur. One is only looking for an order of
magnitude answer, comparable in crudity
to the back-of-the-envelope calculations
of early cosmologists, but our biological
friends tell us, without any apparent
anxiety, that it just can’t be done.’14
As Polkinghorne wrote, attempts were
being made to answer this question15, but
the eye was treated in isolation, neglecting
the more difficult problem of how a brain
evolves that can handle the information
from a more complex eye.
Second, it seemed that simple logic
could replace these demonstrations.
Empirical evidence that variation relevant to evolution is mendelian suggests
that evolution results from changes in
gene frequencies. Because the only cause
496
of adaptive change in allele frequencies
is natural selection, this must direct
adaptive evolution.
Because this logic (or the logic of
natural selection itself) seemed so compelling, and because there were no plausible alternative hypotheses, many biologists were content to assume that available
variation is a ‘sufficient basis on which to
rest, with the all-powerful help of natural
selection, a theory of definite and progressive evolution’16. From 1909 onwards,
too many biologists behaved as if ‘to imagine a use for an organ is … equivalent to
explaining its origin by natural selection
without further enquiry’10. Gould and
Lewontin9 ridiculed this approach as
adaptive ‘storytelling’.
Indeed, some biologists seemed merely
to substitute natural selection for God as
an omnipotent agent of adaptation9.
D’Arcy Thompson observed that ‘To
buttress the theory of natural selection,
the same instances of “adaptation” (and
many more) are used as in an earlier but
not distant age testified to the wisdom of
the Creator’16.
The synthesis would not have developed so loosely if competing alternatives
had been available. Only lack of competition could produce a synthesis where: (1)
many evolutionary biologists, beginning
with Huxley1, failed to distinguish individual advantage from the good of the group
or the species – George Williams17 was the
first to make this distinction generally
recognized; (2) many8,9,18 wondered whether
the synthesis was testable; (3) Gould11
claimed that selection within populations
was irrelevant to macroevolution; and (4)
many failed to distinguish the phenomena
of evolution and adaptation from their
causes. For example, defining adaptations
as characteristics that evolve for their
current functions18 confuses adaptation
with its causes: adaptation should be
defined by the appropriateness of an
organism for its environment, and its
causes treated as a separate question19.
The spread of creationism and antidarwinism reflects from two faults in the
synthesis. First, religious opponents of
the synthesis confuse evolution with its
causes. Because they consider it the synthesis’ weakest link, creationists usually
attack natural selection – the critical issue
for many religious opponents.
I know creationists who became antidarwinians when they learned to distinguish the fact of evolution from its causes.
However, they still refused to help recall a
creationist school board, because it taught
public school students that the development of the universe is visibly controlled
by God. These antidarwinians do not realize that, to most scientists, asserting the
creation of the universe in one go, several
thousand years ago, represents wilful ignorance of the facts. Denying the fact of evolution creates antagonism far greater than
questioning its causes. Confusing evolution with its causes blurs the issues at
stake, creating needless antagonism.
Failure to assess whether natural
selection of random mutations can account
for observed adaptation has spawned
other problems. Because no plausible
scientific alternatives are available, many
scientists think that denying the selection-theory simply withdraws evolution
from the domain of science. However, the
failure to provide clinching evidence
gives antidarwinians no reason to substitute natural selection for God in their
view of the world. Neither have antidarwinians any vested interest in a mechanistic explanation of the origin and evolution of life: if we want them to accept
one, it will have to be convincing.
TREE vol. 14, no. 12 December 1999
PERSPECTIVES
Fisher’s Genetical Theory of
Natural Selection
In his book5, which contributed to the
formation of the synthesis20, Fisher developed a coherent, testable theory of
evolution21,22, with remedies for many of
the difficulties of the synthesis.
Fisher argued that natural selection is
driven by individual advantage, not the
good of the group or the species. He illustrated this distinction by showing that
selection on humans works against the
good of the species. He also showed that
selection on the sex ratio maximizes an
individual’s share of the genes contributed to future generations, but it does
not maximize the population’s growth rate
or its competitive ability. This insight is
fundamental17: one cannot understand the
major transitions of evolution23 without
knowing why, in such transitions, replicating entities benefit from joining groups
that are coherent enough to become
units of selection in their own right24.
He also derived a ‘fundamental theorem of natural selection’, relating evolutionary change to the genetic variation
available. This theorem implies that the
rate of change in the population mean of
a characteristic is the heritable genetic
variance in that characteristic, multiplied
by the proportion by which a unit increase
in this characteristic increases individual
fitness. This theorem is fundamental for
animal breeders25, but Fisher also hoped
to test it under natural conditions.
Finally, Fisher presented several
arguments to show that random mutation
can provide sufficient variation for adaptive evolution. First, his theory of dominance (why, at most loci, heterozygotes
resemble ‘wild-type’ homozygotes) suggests that selection spreads even slightly
advantageous mutations. Second, a crude
model (Box 3) suggests that mutations
are more likely to be favorable when
their effects are small, and the characteristics they affect are simple. The latter
proposition implies that modular organization, in which each locus controls a limited aspect of its organism’s phenotype,
facilitates adaptation. The virtue of modularity is that it allows selection on one
feature without compromising adaptation in others26. Third, Fisher argued
that the only advantage of recombination
is that it allows the simultaneous fixation
of different favorable mutations without
waiting for one mutation to occur on a
chromosome carrying the other. This wait
is appreciable only if mutations of each
type are very rare, as if they occur by
chance rather than by being caused by
some environmental factor. Since recombination is otherwise disadvantageous (it
destroys favorable gene combinations),
the prevalence of sexual reproduction
TREE vol. 14, no. 12 December 1999
Box 4. Fisher and speciation
Antonovics10 has criticized the synthesis for neglecting mechanisms of different modes of speciation;
whereas Mayr27 and Lewontin43 criticized Fisher’s understanding of speciation. I will show that Fisher provided sound leads for understanding mechanisms of speciation, providing another way of demonstrating
the role of evolution by natural selection.
For sexual organisms, Fisher considered three ingredients of speciation: trade-offs, in which increased
ability in one habitat or occupation decreases ability in another; geographical or ecological isolation, in which
a given individual tends to remain in one habitat or occupation; and mate choice. Speciation of two populations
is complete when individuals no longer choose members of the other population as mates, or when such
matings produce no, or sterile, offspring. Fisher defined an asexual species as a population where
descendants of a favorable mutant in one member could competitively replace the descendants of the others.
McMillan et al.39 gave an example where association of mate choice with ecological divergence has
caused speciation in the absence of hybrid breakdown; Seehausen et al.40 demonstrated that mate
choice can initiate sympatric speciation before ecological divergence occurs, citing this as an example of
Fisher’s theory.
Box 5. Fisher, Wright and the synthesis
Although Fisher’s book might show how to construct an effective blueprint for rescuing the synthesis,
Wright’s work makes two crucial contributions towards executing this blueprint.
First, Wright’s work on the complexity of gene interactions indicates that the relative independence in
effect of alleles at different loci within a population, for which there is genetic22 and developmental26 evidence, is a quality that must be selected22. Modularity reflects design, at least partly for the sake of
evolvability26, not intrinsic properties of the raw material.
Second, Wright correctly emphasized the essential role genetic drift can play in creating suitable variation for natural selection. Fisher’s fundamental theorem, as modified by Price35, allows us to show how
eukaryotes and metazoans could evolve24,34 . However, this application of Price’s theorem presupposes
that within-group genetic drift provides the variation for an effective selection among groups24. Thus,
Ford’s44 denial of the evolutionary importance of genetic drift was unhelpful.
Fisher’s unwillingness to see virtues in his opponents’ arguments reduced his effectiveness. The
clearest example is that, when Fisher33 invented a thought experiment that exhibited the ‘cost of sex’22,
he overlooked the importance of his discovery because he was too busy accusing Wright of confusing the
average excess and average effect of a gene substitution.
and recombination implied, in Fisher’s
view, that random mutation produced
abundant favorable variation.
Fisher’s arguments imply that sexual
reproduction and modularity of gene
action reflect how organisms are designed to facilitate evolution by natural
selection of their populations.
Why was Fisher’s book neglected?
Fisher’s book had little influence,
especially in the USA, for several reasons.
First, his mathematics was difficult:
although one can understand Fisher’s
argument without digesting his mathematics, few realized this at the time.
Second, Mayr7, the most influential
architect of the synthesis, consistently
deprecated the contributions of Fisher,
Haldane and Wright, because he27 thought
they had contributed nothing to the
understanding of speciation (Box 4).
Third, Americans interested in evolutionary population genetics, including
Dobzhansky4 and Simpson28, were convinced by Wright’s criticisms of Fisher’s
work. These criticisms were acute, convincing and relevant. Fisher’s theory of
sex assumes that ‘good genes make good
genotypes’, but Wright’s29,30 work on gene
action convinced him that interactions
between loci were so complex that a
genotype’s fitness could not be predicted
from the average fitnesses of its component genes. Asserting the radical dependence of each allele’s expression on alleles
present at other loci contradicted the
importance of the modularity of gene
action implied (but not explicitly formulated) by Fisher. Wright greatly influenced Dobzhansky, who, in turn, greatly
influenced Mayr. Mayr’s31 assault on ‘beanbag genetics’ reflects Wright’s emphasis
on the complexity of gene interactions. Is
modularity simply a theoretician’s dream?
Finally, Fisher was a less effective
controversialist than Wright. Fisher based
his polemic on his theory of dominance,
which Wright demolished convincingly29
and correctly32. He33 also vied with Wright
over who accounted for complex interactions between loci more effectively,
thus undermining his own theory of sex.
Like his opponents, Fisher neglected those
aspects of his book most relevant to the
synthesis. Fisher’s unwillingness to see the
virtues of his opponents’ arguments also
reduced his credibility (Box 5).
The importance of natural selection
in evolution
Identifying fingerprints of the crucial
role of natural selection in macroevolution would reveal the decisive role of
selection in evolution. In many of the
major transitions of evolution23, groups
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
497
PERSPECTIVES
of cooperating entities were transformed
into cohesive higher-level units of selection. Such transitions included: the aggregation of genes into genomes; the transformation of bacteria, containing various
commensal or symbiotic microbes within
their cells, into genuine eukaryotic organisms; the transformation of multicellular
aggregates into true metazoan individuals; and the transformation of insect
groups into cohesive societies with complex divisions of labor. Fisher’s book suggests that group members cooperate only
if each benefits by doing so. For groups
to become cohesive units, an individual’s
advantage must become identical to the
good of its group, or an enforceable community interest must evolve among a
group’s members24. The circumstances,
or mechanisms, making this possible are
the same as those that today suppress
conflicts between the unit and its parts34.
In eukaryotes, organelles must be
subject to effective selection among
groups in the interest of their host cells,
where each group includes organelles of
a given type within a cell. The conditions
that make this possible can be specified
quantitatively from Price’s35 extension of
Fisher’s fundamental theorem. Satisfaction
of these restrictive conditions is an
unmistakeable fingerprint of the role of
natural selection in macroevolution34. By
providing a general means of relating
variation and intensity of selection to
evolutionary change, Fisher’s fundamental theorem of natural selection enabled
Price to compare the effectiveness of
selection at different levels. This comparison enables us to identify many such
fingerprints.
The design of organisms to facilitate
the evolution of their populations provides another reason for believing that
natural selection plays a crucial role in
evolution. One aspect of this design,
already adumbrated by Fisher, is modularity – the restriction of a gene’s action
to a particular ‘compartment’ or facet of
the phenotype26. The importance of modularity in evolution has been illustrated
by the conditions that allow computer
programs to be perfected by testing many
random variants and accepting those
that perform better than their predecessors36. Leigh22, and Gerhart and Kirschner26
summarize genetic and developmental
evidence for this modularity. Recombination and sexual reproduction also contribute to evolvability, as Fisher thought.
The capacity to recombine favorable
mutations is one crucial advantage of recombination, although not the only
one37. Finally, ‘honest’ meiosis, which
enables alleles to spread only if they contribute to the fitness of their bearers, is
crucial for adaptive evolution24.
498
Conclusions
The search for features of organisms
that facilitate evolution by natural selection, which Fisher pioneered so long ago,
has now become a major industry. This
search has become far more effective
now that developmental biology is sufficiently developed to join the evolutionary synthesis26. Evolvability is also playing a major role in attempts to show the
public that Darwin ‘got it right’38.
Acknowledgements
I thank James Crow, Allen Herre,
Betty Smocovitis and two thoughtful
anonymous reviewers for
encouragement and excellent advice.
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