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THE MODERN EVOLUTIONARY THEORY
ERNST MAYR
Museum of Comparative Zoology,
26 Oxford Street, Harvard University, Cambridge, MA 02138
Capstone Address, Presented at the 75th Annual Meeting of
The American Society of Mammalogists, Burlington, VT, June 1995
Of all of Darwin's evolutionary theories,
the one that encountered the greatest resistance, and was therefore the last one to be
accepted, was the theory of natural selection. It was only about 1940 that it was
adopted by the majority of biologists. In order to understand why it encountered this
resistance, it is necessary to survey the history of evolutionary biology. When Darwin, in 1859, proposed his theory of natural
selection, it was opposed at once not by just
one but actually by four different counterproposals. One, of course, was Creationism,
the other three were purely scientific theories, without any invocation of supernatural
factors. These three theories were transmutationism, the claim that evolutionary
novelties originate by major mutations and
by the saltational origin of new kinds of
organisms, and two transformational theories, which explained evolution in terms of
the gradual change of a preexisting entity.
These transformational theories took their
cue from ontogeny, and believed that just
as the fertilized egg is gradually transformed into an adult individual, so an evolutionary lineage is gradually transformed.
There are two very different conceptions of
the nature of this transformation, that is,
how the transformation is caused. One of
them, orthogenesis, is the theory that in the
world of life there is some built-in tendency
or drive toward progression, improvement,
and finally, perhaps, even perfection. The
other, Lamarckism, is based on the belief in
a direct influence of the environment on the
genetic material and an inheritance of acquired characters. From 1859 to about
1940, these three opposing theories were
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actually far more popular than natural selection. In the years from 1930 to 1936,
several leading scholars stated with conviction that each of these opposing theories
had so much support that there was no hope
for a consensus in the near future. Actually,
this was achieved with incredible rapidity
in the 15 years or so, beginning in 1937.
However, before natural selection could
be victorious, the three mentioned countertheories first had to be refuted. I shall say
nothing about Creationism, because with its
reliance on supernatural forces, it is outside
the realm of scientific investigation. But
how were the other three counter-theories
refuted? Let me begin with saltationist
transmutationism. This was the theory of
evolution that was supported by all essentialists. They simply couldn't see how one
could get from one type to another type
without a saltation.
This theory was popular from Darwin's
time on. It was supported by T. H. Huxley,
also by some leading German biologists,
and it had support from the early Mendelians, because Bateson, de Vries, and Johannsen were saltationists. And as late as
1940 and 1950 it had suppofiers among paleontologists, and in Goldschmidt and the
botanist Willis. This theory was refuted
when evolutionists pointed out that organisms are not types but populations, and that
no population as a whole could ever be converted into a new type by a single step. Furthermore, since an organism is controlled
by an elaborate and harmonious genotype,
it is quite inconceivable to expect that a
new viable harmonious genotype could be
produced by a single step. Goldschmidt
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frankly admitted that ordinarily such saltations would only produce "monsters," but
he expressed his faith that once in a while
there would be a "hopeful monster" that
would indeed be adapted for some new ecological niche. However, it was shown by the
naturalists that the large quantity of unsuccessful mutations that was postulated by the
saltationists could not be found. More importantly, the naturalists showed through
the study of geographic speciation that the
origin of new species was a gradual process, as had been postulated by Darwin, and
that there was no need to invoke saltations.
The post-Mendelian generation of geneticists also showed that the frequency of viable large mutations was very low, and that
most mutations were very small and not in
any way able to produce the kind of transmutationist novelties. Both B. Rensch and
G. G. Simpson showed that morphologists
could explain macroevolution without difficulty in terms of selection and very small
mutations. And that was the end of transmutationism.
The second of the opposing explanatory
schemes was orthogenesis. Among orthogenetic theories were nomogenesis of the
Russian E. S. Berg, aristogenesis of H. R
Osborn, and the omega principle of Teilhard de Chardin. Its supporters believed
that there was a built-in tendency in evolutionary lineages toward ever greater complexity and perfection. However, neither
could the geneticists find any genetic mechanism that could make such a tendency toward perfection possible, nor did the analysis of the paleontologists support the claim
of a steady trend toward perfection. Indeed,
one encountered reversals and rather drastic
shifts to new directions in most well-analyzed evolutionary lineages.
So-called excess structures such as the
antlers of the Irish elk and the tusks of the
Babirussa were claimed by the orthogenesists to be obviously deleterious developments that could be explained only by the
existence of a non-stoppable trend. However, it was shown by the Darwinians that
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the antlers of the Irish elk, supported by
sexual selection, were by no means excessive, and furthermore could also be explained in part by allometry, that is, the correlated growth of a structure with an increase in body size. Orthogenesis, of
course, was in a way a byproduct of the
prevailing deterministic thinking of this period and became unpopular when the shortcomings of determinism were revealed.
In the last analysis, the whole orthogenesis concept was a misguided analogy with
ontogeny. The proponents of orthogenesis
thought that just as in ontogeny eventually
the adult characters arise inevitably, so evolution also was in a way programmed and
would ultimately lead to certain end results
that had been programmed in their genotype from the beginning. The Darwinians
countered this argument by pointing out
that evolution was not the gradual transformation of a type but was a populational
phenomenon. This Darwinian concept of
evolution was completely opposed to the
conceptual framework of the orthogenesists. The frequency of extinction and the
equally high frequency of ultimately deleterious evolutionary pathways demonstrate
the improbability of such orthogenetic programs particularly well. Of course, the genetic analysis after 1910 found no evidence
whatsoever for the existence of any orthogenetic programs.
Finally, there was the school believing in
a direct effect of the environment and in an
inheritance of acquired characters. They believed that the genetic material was plastic
and their genetic theory was referred to as
the theory of soft inheritance. This theory
was rather thoroughly refuted by Weismann
as early as 1883, but continued to have support. This support was particularly strong in
the early years of this century owing to the
saltationist claims of the Mendelians and
their opposition to natural selection. Anyone believing in gradual evolution, as did
most of the naturalists, was almost forced
to accept Lamarckism although, like Darwin, at the same time also accepting natural
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selection. The main contribution made by
the inheritance of acquired characters, according to this school, was to supply abundant variation to serve as material for natural selection. Darwin himself, of course,
believed in an inheritance of acquired characters, and many of the later Lamarckians
also believed in natural selection and actually considered themselves to be good Darwinians.
A major target of the opposition was
Darwin's claim that all evolutionary
change, and particularly adaptation, is controlled by natural selection. If we assume
that a structure or behavior or any attribute
of an organism is adapted, it follows that it
must have been incorporated into the genotype owing to natural selection. The opposition of the anti-Darwinians was not so
much based on concrete evidence as on an
intuitive aversion to the so-called "mechanistic" Darwinian interpretation and to the
large role of chance in the Darwinian explanation.
Even though Weismann in 1883 had denied categorically any existence of an inheritance of acquired characters, naturalists,
and in fact, almost all evolutionary biologists still more or less believed in it for another 50 years. Some of them devoted many
years to experimentation to prove it. All experiments, however, turned out to be negative. Furthermore, the detailed genetic analysis, beginning in 1910 in Morgan's laboratory, found no evidence for it whatsoever.
The most decisive refutation, however, was
eventually supplied by molecular biology
when it showed that information could be
transferred from nucleic acids to proteins,
but no information could be transferred
from the proteins of the body to the nucleic
acids of the germplasm. This is called the
central dogma of molecular biology.
During the first quarter of the 20th century the support for the three non-Darwinian evolutionary theories, saltationism, orthogenesis, and Lamarckian inheritance was
far greater than the support for natural selection. Indeed, natural selection was not
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widely adopted until these three competing
theories had been thoroughly refuted.
The credit for the decisive refutation of
the three non-Darwinian explanations of
evolution is shared by genetics, systematics,
and paleontology. The defeat of the nonDarwinian theories during the synthesis
was so complete that since about 1950 no
creditable author has come out to support
any of them. At the present time, there are
no longer any serious followers of saltationism, orthogenesis, or an inheritance of
acquired characters.
THE EVOLUTIONARY SYNTHESIS
Much of the refutation of the non-Darwinian theories took place already prior to
1935, and yet, there still didn't seem to be
any signs of a consensus among the evolutionary biologists. One could recognize
two major camps of Darwinians at that
time, and in fact, even today these two
camps can still be distinguished. The one
camp is that of the laboratory geneticists
who study evolution with the help of experimentation and mathematical models.
The other camp consists of the naturalists
whose interpretation of evolution is based
on the study of populations in the field. In
1935 there was still a rather strong saltationist bias in the thinking of the geneticists, a remnant of the thinking of the early
Mendelians, while owing to their strong
emphasis on the gradualness of evolution
there was still a tendency among the naturalists to believe in soft inheritance, that is,
the capacity of the genome to be affected
by the environment.
The two camps were quite suddenly
brought together to a consensus through the
publication in 1937 of Dobzhansky's Genetics and the Origin of Species. Dobzhansky was the ideal person to initiate the reconciliation of the two camps because he
himself actually belonged to both of them.
By background he was a naturalist, and
while still in Russia he was a taxonomist of
a group of beetles, the Coccinellidae. In
1927, he came to the United States and
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worked for 10 years in the laboratory of T.
H. Morgan, where he became thoroughly
acquainted with the thinking of the geneticists.
Perhaps I should describe the differences
in the thinking of the two camps in a little
more detail. The geneticists were strict reductionists. For them the gene was the target of selection, and they were only interested in, and able to investigate what happens in a given gene pool, that is, the origin
and maintenance of adaptedness. Their concept of evolution was, so to speak, a vertical one, that is, relating to the changes that
happen over time in a given gene pool.
The naturalists-taxonomists differed by
considering the individual as a whole as the
target of selection. For them the population
was the unit of evolution. Their chief interest was the origin of diversity. They developed the new biological species concept,
they solved the riddle of speciation through
the theory of geographic speciation, and
they demonstrated a continuity between
speciation and macroevolution. For them all
evolution was populational, except for a
few special phenomena such as polyploidy,
and therefore all evolution by necessity was
gradual.
The naturalists were at that time still
rather unaware of the drastic changes in the
thinking of the geneticists between the time
of Mendelism and the 1930s, and in particular with the shift in the genetic concept of
mutation. Because the geneticists were always working with a single population, a
single gene pool, they in turn were quite
unaware of the variation of populations and
of the problems connected with the origin
of organic diversity.
Dobzhansky in his Genetics and the Origin of Species (1937) presented the views
of both camps. He showed that there was
no conflict between their ideas. Furthermore, he showed that they very happily
complemented each other, and that the gaps
in the theories of the geneticists were filled
by the theories of the naturalists and vice
versa. Dobzhansky's thesis was soon taken
up by the other so-called architects of the
evolutionary synthesis, Julian Huxley, Ernst
Mayr, and G. G. Simpson, in Germany by
Rensch, and in botany by Stebbins.
The long set of controversies, that had
begun with the publication of Darwin's
Origin of Species in 1859, was now terminated after 80 years and there was a remarkable consensus in the early symposia
after 1937. It was obvious that a synthesis
of concepts had taken place in evolutionary biology. But actually, as several recent
historians have pointed out, the impact of
this synthesis extended way beyond evolutionary biology. Indeed, the synthesis
achieved a unification of all of biology.
This was perhaps best expressed by Dobzhansky in his well known saying, "Nothing in biology makes sense except in the
light of evolution."
Eventually, the synthesis was joined even
by the developmental biologists who had opposed Darwinism at least up to the 1960s.
One might think that the almost explosive development of molecular biology after 1953 might have led to a drastic revision
of the beliefs of the evolutionary synthesis,
but this did not take place. As Maynard
Smith had convincingly demonstrated, molecular biology was an almost continuous
and gradual change from classical genetics.
At the very beginning this was not so obvious because the first molecular biologists
were actually biochemists and were, on the
whole, rather hostile toward biology. But as
the next generation of molecular biologists
developed, most of them trained as biologists, this hostility disappeared, and now almost every molecular biologist includes
evolutionary studies in his program, because by now everybody knows that biological macromolecules experience as much
evolution as does any macroscopic organ
system.
ACHIEVEMENTS
What the synthesis also achieved was a
substantial clarification of all Darwinian
concepts.
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Let us begin with natural selection. His
opponents at first referred to Darwin's theory as "evolution by accident." This is, of
course, a total misconception. We now
know that natural selection is a two-step
process. The first step produces genetic
variation and Darwin, from the beginning,
postulated the availability of an enormous
amount of variation in populations. Darwin
did not know where it came from but he
knew it was there. He even erroneously invoked soft inheritance to generate some of
this variation.
The geneticists always attributed variation to mutation and ultimately, of course,
this is indeed the source of all genetic variation. But the genotypic difference between
one generation and the next is mostly the
product of genetic recombination. But
whether due to mutation or to recombination, the variational difference between one
generation and the next is entirely due to
chance, except for some instances of socalled biased variation, which I do not have
time to discuss.
The second step is that of the real selection. Darwin's choice of the metaphor selection was not altogether a happy one. He
was at once asked: who selects? Darwin
said "nature." Well, said his opponents,
this is the same agent we call God.
Herbert Spencer saw the weakness in
Darwin's terminology and suggested instead an emphasis on survival. But the formulation "survival of the fittest" was also
attacked as being circular: who are the fittest?-those who survive.
A good replacement description of natural selection is "non-random elimination."
Selection, then, is the elimination of the less
well adapted individuals, hence obviously a
non-random elimination. Evolutionists had
long distinguished a normalizing selection,
which was exactly the elimination of all
less well adapted individuals. The new metaphor simply says that all selection is normalizing selection, except that every generation may have its own norm, determined
by the prevailing environment of the mo-
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ment. There is no trace of circularity in this
formulation.
The wording "non-random elimination"
also makes it clear that Darwin's natural selection is not a teleological process. It never
has a definite goal; there is always a chance
component in the selection of the lucky survivors.
SPECIATION
It is one of the great ironies in the history
of biology that Darwin failed to settle the
problem of speciation in the volume entitled On the Origin of Species. He had the
right solution in his early writings from
1837 to about 1852, but then he got all confused by not realizing tha~ he applied the
term 'varieties' to two entirely different
phenomena. We now know that speciation
in sexually reproducing organisms is normally a populational process, that is, the acquisition of isolating mechanisms by a population. And normally this can only ha.ppen
in geographic isolation.
What has become clear since the evolutionary synthesis is that there are actually
two forms of geographic speciation. Speciation by secondary isolation, also referred
to as the dumbbell model of speciation,
takes place when a widespread species is
cut through by a newly arisen barrier, either
water or an unsuitable vegetation belt, and
the two. isolated portions become two species. The Pleistocene ice and climate in the
Mississippi Valley produced a large number
of such species pairs in refuges east and
west of the Mississippi, even though the
isolation was often not long enough for the
speciation process to be completed, resulting in widespread hybrid belts such as between yellow shafted and red shafted flickers.
The other process of speciation, speciation by primary isolation, also called peripatric speciation, occurs when a founder
population is established beyond the periphery of the species range and gradually
evolves into a new species, owing to the
acquisition of isolating mechanisms. The
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special aspect of founder populations is that
they usually have only a small fraction of
the genes of the parental population, and
then are exposed both to inbreeding and entirely new selection pressures. As a result,
such a population has a chance to shift to
an entirely new adaptive zone, accompanied by drastic genetic restructuring.
This is why peripatric speciation is so
important for macroevolution. The recently
published detailed analysis of the evolution
of fossil bryozoans is completely consistent
with this theory of speciational evolution,
called by Eldredge and Gould the theory of
punctuated eqUilibrium.
At this mammal meeting I will not discuss sympatric speciation because there are
no niches of mammal species that would be
suitable for sympatric speciation. Even in
insects where a shift to a new host plant
would seem to make sympatric speciation
possible, the evidence is still ambiguous.
AFfER THE SYNTHESIS
One of the totally unanticipated byproducts of the synthesis was the unification of
biology, but this is now considered by some
philosophers of science to be the most important achievement of the synthesis. But,
was the synthesis really a success as far as
evolution is concerned?
How complete was the synthesis of the
two opposing camps of the early 1930s?
Well, I am afraid one must admit that it was
not entirely complete. The naturalists still
considered the individual-as-a-whole to be
the major target of selection, while the geneticists, for the sake of their calculations,
preferred to consider the gene as this target.
Therefore, they left out of their calculations
all the evolutionary consequences of the interaction of different genes. In fact, even
today most of the geneticists ignore a fact,
which has been established many times,
namely that the same gene may have a different selective value in one genotype than
in another one.
The emphasis on the gene also is responsible for the so-called theory of neutral evo-
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lution. Kimura and others showed that some
mutational allele replacements have no effect on the fitness of the new genotype. He
called such changes neutral mutations and
refers to their incorporation into the genotype as neutral evolution. However, there is
obviously no selection of such neutral mutations. They are simply accidental members of successful genotypes, and even
though the genotype on which they became
part of the popUlation, was favored by selection, the neutral genes only came along,
so to speak, as hitchhikers. Such neutral
mutations are evolutionary "noise" rather
thim evolution. By concentrating on single
genes rather than on individuals-as-awhole, geneticists also have more difficulty
in studying bottleneck effects as well as the
role of inbreeding in very small populations.
A second area where the synthesis has
not yet been entirely successful is the replacement of typological by population
thinking. This is most evident in physical
anthropology where Australopithecus africanus, Homo habilis, Homo erectus, and
other formerly existing hominid taxa are
still conceived of rather typologically. The
same is true in much of paleontology. And
typological thinking is still rather widespread in the study of microorganisms and
fungi, in part by necessity, because asexual
organisms do not form Mendelian populations.
What is most characteristic for science is
the steady advance in our theories and our
thinking. It is therefore quite legitimate to
ask questions about the future of the evolutionary synthesis. For instance, has any
part of the synthesis been refuted, as has
been claimed by quite a few critics? The
clear answer is no. The so-called theory of
punctuated equilibria, for instance, is merely an elaboration of my own theory of speciational evolution, published in 1954.
There I pointed out quite clearly that this is
a populational theory, and even though it
results in a rather remarkable speeding up
of evolution, it is not saltational at all and
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MAYR-CAPSTONE ADDRESS
is nowhere in the slightest conflict with the
synthesis.
The next question we can ask is whether
any other evolutionary theory has been proposed in the last 50 years that would seem
to be a threat to the evolutionary synthesis.
The answer again is no. No such theory has
ever been proposed.
Finally, one might ask whether there are
any parts of the existing Darwinian theory
that look as if they were in need of replacement? Again I must say no. To be sure,
there are still large areas in biology where
our knowledge is incomplete, one might
even say quite insufficient. However, invariably this has to do with the properties
of complex systems. The three systems that
are particularly obvious in this respect are
first the neuronal system of the brain, the
second, the problem of the translation of the
genetic program of the fertilized egg
through development into the adult organism, and third, the interactions that occur
within an ecosystem.
Whatever the solution to these three great
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sets of problems will be, I am quite convinced that none of these solutions will be
in any conflict whatsoever with the theory
structure of the evolutionary synthesis.
It is therefore no exaggeration to claim
that the evolutionary synthesis was one of
the most remarkable and successful events
in the history of biological science.
Thank you.
Addendum by Ernst Mayr, 14 September
1995. To those who want to make a more
thorough study of the history of modern
evolutionary theory, I recommend these
books.
D. (ED.) 1985. The Darwinian heritage. Princeton University Press, Princeton, New Jersey, 1138
pp.
MAYR, E. 1982. The growth of biological thought:
diversity, evolution, and inheritance. The Belknap
Press of Harvard University Press, Cambridge, Massachusetts, 974 pp.
- - - . 1988. Toward a new philosophy of biology:
observations of an evolutionist. The Belknap Press
of Harvard University Press, Cambridge, Massachusetts, 564 pp.
- - - . 1991. One long argument. Charles Darwin
and the genesis of modern evolutionary thought.
Harvard University Press, Cambridge, Massachusetts, 195 pp.
KOHN,