AN ECOLOGY OF REPLICATORS

RICHARD DAWKINS

Daniel Dennett went only a little too far when he wrote, at the beginning
of Darwin’s Dangerous Idea (1995): “Let me lay my cards on the table. If I
were to give an award for the single best idea anyone has ever had, I’d
give it to Darwin, ahead of Newton and Einstein and everyone else.”
He wasn’t talking about evolution itself, which was not Darwin’s idea,
but natural selection, which pretty much was. Today, notwithstanding
local school boards in various backwoods and boondocks of the United
States, no educated person doubts the truth of evolution. Nor do they
doubt the force of natural selection. Natural selection is not the only driver
and guide of evolution. At least at the molecular level, random drift is also
important (Kimura 1983) but selection is the only force capable of produc-
ing adaptation. When it comes to accounting for the stunning illusion of
design in nature, there is no alternative to natural selection. The one idea
that might, for a moment, have seemed to be a conceivable alternative,
Lamarckism, is not, as has sometimes been suggested, a good alternative
theory which just had the misfortune to be false. It isn’t even a good
alternative theory. The Lamarckian theory is not a big enough theory to
account for adaptation. It couldn’t work, even on some hypothetical
planet where acquired characteristics were inherited (Dawkins 1982a).
If a biologist denies the importance of natural selection in evolution, it
is pretty safe to assume not that he has some alternative theory but that he
simply underrates adaptation as a dominant property of life that needs
explaining (Mayr 1983). Probably he has never set foot in a tropical rain
forest, or set flipper over a coral reef, or set eyes on a David Attenborough
film.
Nowadays, questions about adaptation are high in the consciousness
of field biologists. It has not always been so. My old maestro Niko Tinber-
gen (1963) wrote of an experience when he was a young man: “I still
remember how perplexed I was upon being told off firmly by one of my
zoology professors when I brought up the question of survival value after
he had asked ‘Has anyone an idea why so many birds flock more densely
when they are attacked by a bird of prey?’”

Oxford University Museum of Natural History, Parks Road, Oxford OXI 3 PW, UK.
[email protected]

Ludus Vitalis, vol. XII, num. 21, 2004, pp. 43-52.

44 / LUDUS VITALUS / vol. XII / num. 21 / 2004

Today’s student is more likely to be perplexed about what the professor

could possibly have meant by his question if not survival value. People in
Tinbergen’s own field of ethology now complain of a stampeding backlash
in the other direction, towards an overwhelming preoccupation with
Darwinian survival value, at the expense of studies of behavioral mecha-
nisms.
But still when I was learning biology at school, we were warned against
a dire sin called ‘teleology’. This was actually a warning against Aristote-
lian final causes, not against Darwinian survival value. Nevertheless, it
perplexed me because I had never found final causes the slightest bit tempt-
ing. Any fool can see that a ‘final cause’ is not a cause at all. It is just another
name for the problem which, eventually, Darwin solved. Darwin showed
how the illusion of a final cause could be produced by comprehensible
efficient causes. His solution is the only workable one that has ever been
suggested, and my hunch is that it will never be superseded. It has of
course been refined, by the giants of the Modern Synthesis including Ernst
Mayr. Darwin and his twentieth century successors have solved biology’s
deepest mystery: the source of the illusion of design which pervades the
living, but not the nonliving world.
The illusion of design is at its strongest in the body shapes and behavior
patterns, the tissues and organs, the cells and molecules of individual
creatures. The individuals of every species, without exception, show it
powerfully. But there is another illusion of design which we notice at a
higher level: the level of ecology. Design seems to reappear in the dispo-
sition of species themselves, in their arrangement into communities and
ecosystems, in the dovetailing of species with species in the habitats which
they share. There is a pattern in the intricate jigsaw of rainforest, say, or
coral reef, which leads rhetoricians to preach disaster if but one compo-
nent should be untimely ripp’d from the whole.
In extreme cases, such rhetoric takes on mystical tones. The womb is of
an earth goddess, all life her body, the species her parts. Yet, without
giving in to such hyperbole, there is a strong illusion of design at the
community level, less compelling than within the individual organism but
worth attention. The animals and plants that live together in an area seem
to fit one another with something like the glove-like intimacy which the
parts of an animal display as they mesh with other parts of the same
organism.
A cheetah has the teeth of a carnivore, the claws of a carnivore, the eyes,
ears, nose and brain of a carnivore, leg muscles that are suitable for chasing
meat, and guts that are primed to digest it. Its parts are choreographed in
a dance of carnivorous unity. Every sinew and cell of the big cat has
meat-eater inscribed through its very texture, and we can be sure that this
extends deep into the details of biochemistry. The corresponding parts of
 DAWKINS / AN ECOLOGY OF REPLICATORS / 45

an antelope are equally unified with each other, but in pursuit of a

different route to survival. Guts designed to digest plant roughage would
be ill-served by claws and instincts designed to catch prey. And viceversa.
A hybrid between a cheetah and an antelope would fall flat on its evolu-
tionary face. Tricks of the trade cannot be cut from one and pasted into
the other. Their compatibility is with other tricks of the same trade.
Something similar can be said of communities of species. The language
of the ecologist reflects this. Plants are primary producers. They trap
energy from the sun, and make it available to the rest of the community,
via a chain of primary, secondary and even tertiary consumers, culminat-
ing in scavengers. Scavengers play a recycling ‘role’ in the community.
Every species, in this view of life, has a ‘role’ to play. In some cases, if the
performers of some role, such as scavengers, were removed, the whole
community would collapse. Or its ‘balance’ would be upset and it might
fluctuate wildly, out of ‘control’ until a new balance is set up, perhaps with
different species playing the same roles. Desert communities are different
from rainforest communities and their component parts are ill-suited to
other such communities just as—or so it seems—herbivorous colons are
ill-suited to carnivorous teeth or hunting instincts. Coral reef communities
are different from sea bottom communities, and their parts cannot be
exchanged. Species become adapted to their community, not just to a
particular physical region and climate. They become adapted to each
other. The other species of the community are an important—perhaps the
most important—feature of the environment to which each species be-
comes adapted. In one sense, the other species of the ecosystem are just
another aspect of the weather. But unlike the temperature and the rainfall,
the other species are themselves evolving. The illusion of design in eco-
systems is an inadvertent consequence of this coevolution.
The harmonious role-playing of species in a community, then, resem-
bles the harmony of the parts of a single individual organism. The resem-
blance is deceptive and must be treated with caution. We must not fall for
the excesses of group selectionist panglossianism such as the ludicrous
concept of ‘prudent predators’ (Slobodkin 1961). Given my biases, it feels
like pulling teeth to say so, but the analogy between organism and com-
munity is not completely without foundation. It is one of my purposes in
this article to argue that there is an ecology within the individual organism.
I am not making the now commonplace point that a large metazoan body
contains a community of bacteria, including mitochondria and other
modified bacteria. I am making the much more radical suggestion that we
should recognize the entire gene pool of a species as an ecological com-
munity of genes. The forces that produce harmony among the parts of an
organism’s body are not unlike the forces that produce the illusion of
harmony in the species of a community. There is balance in a rainforest,
46 / LUDUS VITALUS / vol. XII / num. 21 / 2004

structure in a reef community, an elegant meshing of parts whose coevo-

lution recalls coadaptation within an animal body. In neither case is the
balanced unit favored as a unit by Darwinian selection. In both cases the
balance comes about through selection at a lower level. Selection doesn’t
favour a harmonious whole. Instead, harmonious parts flourish in the
presence of each other, and the illusion of a harmonious whole emerges.
A helpful language for explaining the emergence of such harmony is the
game-theoretic language of evolutionary stability (Maynard Smith 1982).
At the individual level, to rehearse an earlier example in genetic lan-
guage, genes that make carnivorous teeth will flourish in a gene pool
containing genes that make carnivorous guts and carnivorous brains, but
not in a gene pool containing genes for herbivorous guts and brains. At
the community level, an area that lacks carnivorous species might experi-
ence something similar to a human economy’s ‘gap in the market.’ Car-
nivorous species that enter the area find themselves flourishing. If the area
is a remote island which no carnivorous species has reached, or if a recent
mass extinction has devastated the land and created a similar gap in the
market, natural selection will favour individuals within non-carnivorous
species that change their habits and eventually their bodies, and become
carnivores. After a long enough period of evolution, specialist carnivore
species will be found to have descended from omnivorous or herbivorous
ancestors.
Carnivores flourish in the presence of herbivores, and herbivores flour-
ish in the presence of plants. But what about the other way around? Do
plants flourish in the presence of herbivores? Do herbivores flourish in the
presence of carnivores? Do animals and plants need enemies to eat them
in order to flourish? Not in the straightforward way that is suggested by
the rhetoric of some ecological activists. No creature benefits directly from
being eaten. But grasses that can withstand being cropped better than rival
plant species, really do flourish in the presence of grazers—on the princi-
ple of ‘my enemy’s enemy.’ And something like the same story might be
told of the victims of parasites—and predators, although here it is more
complicated. It is still misleading to say that a community ‘needs’ its
parasites and predators like a polar bear needs its liver or its teeth. But the
enemy’s enemy principle does lead to something like the same result. It
can be right to see a community of species as a kind of balanced entity
which is potentially threatened by removal of any of its parts.
The idea of community, as made up of lower level units that flourish in
the presence of each other, pervades life. But, as I have said, I want to go
beyond the familiar point that animal cells are communities of hundreds
or thousands of bacteria. This is not to downplay the importance of
bacterial symbioses. Mitochondria and chloroplasts have become so com-
prehensively integrated into the smooth workings of the cell that their
 DAWKINS / AN ECOLOGY OF REPLICATORS / 47

bacterial origins have only recently become understood. Mitochondria are

as essential to the workings of our cells as our cells are to them. Their genes
have flourished in the presence of ours as ours have flourished in the
presence of theirs. Plant cells by themselves are incapable of photosynthe-
sis. That chemical wizardry is performed by guest workers within the cells,
originally bacteria and now relabelled chloroplasts. Plant eaters such as
ruminants and termites are themselves largely incapable of digesting
cellulose. But they are good at finding and chewing plants. The gap in the
market offered by their plant-filled guts is exploited by symbiotic micro-
organisms who possess the biochemical expertise necessary to digest plant
material efficiently, and to the benefit of their herbivorous hosts. Creatures
with complementary skills flourish in each other’s presence.
My point is that the process is mirrored at the level of every species’
‘own’ genes. The entire genome of a polar bear or a penguin, of an iguana
or a guanaco, is a set of genes that flourish in each other’s presence. The
immediate arena of this flourishing is the interior of an individual’s cells.
But the long-term arena is the gene pool of the species. Given sexual
reproduction, the gene pool is the habitat of every gene as it is recopied
and recombined down the generations.
This gives the species its singular status in the taxonomic hierarchy.
Nobody knows how many separate species there are in the world, but,
thanks largely to Ernst Mayr, we at least know what it would mean to
count them. Arguments about whether there are 30 million separate
species, as some have estimated, or only 5 million, are real arguments
(Wilson 1992). The answer matters. Arguments about how many genera
there are, or how many orders, families, classes or phyla have no more
status than arguments about how many tall men there are. It’s up to you
how you define tall, and it is up to you how you define a genus or a family.
But—as long as reproduction is sexual—the species has a definition which
goes beyond individual taste, and does so in a way that really matters.
Fellow members of a species participate in the same shared gene pool. The
species is defined as the community whose genes share that most intimate
of arenas for cohabitation, the cell nucleus—a succession of cell nuclei
through generations.
When a species spawns a daughter species, usually after a period of
accidental isolation, the new gene pool constitutes a new arena for inter-
gene cooperation to evolve. All the diversity on earth has come about
through such splittings. Every species is a unique entity, a unique set of
coadapted genes, cooperating with each other in the enterprise of building
individual organisms of that species. The gene pool of a species is an edifice
of harmonious co-operators, built up through a unique history. Any gene
pool, as I have argued elsewhere, is a unique written record of ancestral
history. Slightly fanciful perhaps, but it follows indirectly from Darwinian
48 / LUDUS VITALUS / vol. XII / num. 21 / 2004

natural selection. A well-adapted animal reflects, in minute detail even

down to the biochemical, the environments in which its ancestors sur-
vived. A gene pool is carved and whittled through generations of ancestral
natural selection, to fit that environment. In theory a knowledgeable
zoologist, presented with the complete transcript of a genome, should be
able to reconstruct the environmental circumstances that did the carving.
In this sense the DNA is a coded description of ancestral environments, a
‘genetic book of the dead’ (Dawkins 1998, chapter 10). George Williams
(1966) had already said it more economically: “A gene pool is an imperfect
record of a running average of selection pressures over a long period of
time in an area often much larger than individual dispersal distances.”
The gene pool of a species, then, is the rainforest in which the ecology
of the genes flourishes. But why have I called my article an ecology of
replicators? In answering this, I need to step back and look at a controversy
in evolutionary theory, one in which Ernst Mayr has been an eloquent
partisan. It is the controversy over the unit in the hierarchy of life at which
natural selection may be said to act. In Richard Alexander’s phrase, “The
fittest what?” Ernst Mayr and I have both coined a word—‘Selection’ in his
case, ‘Optimon’ in mine—for the sole purpose of asking the question “What
is the entity about which you may say that an adaptation is good for it?”
Is it for the good of the group, the individual, the gene, life as a whole, or
what? My own answer to the question—the gene—is not the answer Ernst
Mayr would give—the organism. I shall try to show that the difference is
apparent, not real. It will disappear when terminological differences are
sorted out. After such presumptuous—not to say impertinent—promise,
let me try to deliver on it.
The wrong way to set up the debate is as a competition between rungs
on a ladder, of which the gene is the lowest: gene, cell, organism, group,
species, ecosystem. What is wrong with the ladder of levels is that the gene
is really in an entirely different category from all the rest. The gene is what
I have called a replicator. All the rest are, if anything, ‘vehicles’ for repli-
cators. The justification for treating the gene as special in this list of levels
was clearly presented by Williams in 1966:

The natural selection of phenotypes cannot in itself produce cumulative

change, because phenotypes are extremely temporary manifestations The
same argument holds for genotypes... Socrates’ genes may be with us yet, but
not his genotype, because meiosis and recombination destroy genotypes as
surely as death... It is only the meiotically dissociated fragments of the geno-
type that are transmitted in sexual reproduction, and these fragments are
further fragmented by meiosis in the next generation. If there is an ultimate
indivisible fragment it is, by definition, ‘the gene’ that is treated in the abstract
discussions of population genetics.
 DAWKINS / AN ECOLOGY OF REPLICATORS / 49

Philosophers now call this “genic selectionism,” (Sterelny and Kitcher

1988) but I doubt that Williams regarded it as a radical departure from
orthodox neo-Darwinian ‘individual selection’. Nor did I, when I reiter-
ated and extended the same argument a decade later in The Selfish Gene
and The Extended Phenotype. We thought we were just clarifying what
orthodox neo-Darwinism really meant. Yet both critics and supporters
misunderstood our view as an attack on the Darwinian idea of the indi-
vidual organism as the unit of selection. This was because we had not then
made sufficiently clear the distinction between replicators and vehicles. Of
course the individual organism is the unit (or at least a very important
unit) of selection if you mean unit in the sense of vehicle. But it isn’t a
replicator at all.
A replicator is anything of which copies are made. An individual organ-
ism is not a replicator in this sense, and individual reproduction is not
replication. Not even where it is asexual, clonal reproduction. This is not
a matter of fact but a matter of definition. If you doubt it, you have not
grasped the significance of the term ’replicator’.
For an operational criterion for whether an entity is a true replicator,
ask what is the fate of blemishes in entities of this class. An individual
organism, such as a clonally reproducing aphid or stick insect, would be
a true replicator only if blemishes in the phenotype—say an amputated
leg—were reproduced in the next generation. And of course they are not.
Note that a blemish in the genotype—a mutation—is reproduced in the
next generation. Of course it may then show itself in the phenotype too,
but it is not the phenotypic blemish itself which is copied. This is no more
than the familiar principle of the non-inheritance of acquired charac-
teristics, or—its molecular version—Crick’s Central Dogma (1958).
There could be a form of life on some distant planet where individual
reproduction really is true replication. This would be so if the body were
scanned, say by some biological version of magnetic resonance imaging,
and every atom of the original parent copied in manufacturing the off-
spring. Needless to say, this is not what happens in any life form known
to us. But the informational equivalent does happen to germ-line DNA.
I have described (Dawkins 1982b) a replicator as ‘active’ if something
about its nature affects its proficiency in being copied, which implies that
blemished replicators may be less proficient, or more proficient than the
original (in practice because of what we are accustomed to calling ’pheno-
typic effects’). The true unit of selection in any Darwinian process, on any
planet, is an Active Germ-line Replicator. On this planet, it happens to be
DNA.
Williams has returned to the matter in his more recent book, Natural
Selection: Domains, Levels and Challenges (1992). He agrees that the gene
does not belong in the same hierarchical list as the organism: “These
50 / LUDUS VITALUS / vol. XII / num. 21 / 2004

complications are best handled by regarding individual selection, not as a

level of selection in addition to that of the gene, but as the primary
mechanism of selection at the genic level.”
‘Primary mechanism of selection at the genic level’ is Williams’s way of
saying what I would call the ‘vehicle’, and David Hull (1980) would call
the ‘interactor’. Williams’s version of my ‘replicator’—in other words his
way of singling out the gene from all vehicles—is to coin the phrase codical
domain, as opposed to material domain. A member of the codical domain is
a codex. The information coded in a gene is firmly in the codical domain.
The atoms in the DNA of the gene are in the material domain. The only
other candidates I can think of for the codical domain are self-replicating
computer programs, and units of cultural inheritance. Which is to say that
both these are candidates for the title of Active Germ-line Replicator, and
candidates for the basic unit of selection in a hypothetical Darwinian
process. The individual organism is not even a candidate for a replicator
in any Darwinian process, however hypothetical.
But I haven’t yet done justice to the criticisms of the idea of genic
selectionism. The most cogent of these criticisms have come from Ernst
Mayr himself, using arguments foreshadowed in his famous attack on
beanbag genetics, and in the ‘Unity of the genotype’ chapter of Animal
Species and Evolution. In that chapter, for example, he said: “To consider
genes as independent units is meaningless from the physiological as well
as from the evolutionary viewpoint.”
This beautifully written book is a favourite of mine, and I agree with
every word of the ’Unity of the genotype’ chapter except its take-home
message, which I disagree with profoundly!
The important thing is to distinguish between the role of genes in
embryology and the role of genes in evolution. It is undeniably the
case—but completely irrelevant to the levels of selection debate—that
genes interact with each other in inextricably complex ways in embryol-
ogy, even if not all embryologists would go so far as Mayr (1963) in saying:
“Every character of an organism is affected by all genes and every gene
affects all characters.”
Mayr himself acknowledges that this was exaggerated. I am happy to
quote it in the same spirit. Happy to quote it because, even if it were
literally true, it would not undermine, not even to the tiniest extent, the
status of the gene as the unit of selection: unit in the sense of replicator,
that is. If this sounds like a paradox, the resolution is actually given by
Mayr himself (1963): “A given gene has as its genetic environment not only
the genetic background of the given zygote on which it is temporarily
placed, but the entire gene pool of the local population in which it occurs.”
This really is the key point. Every gene is selected for its ability to survive
in its environment. We naturally think first of the external environment.
 DAWKINS / AN ECOLOGY OF REPLICATORS / 51

But the most important elements in the environment of a gene are the
other genes. This ‘ecology of genes’, in which each is separately selected
for its ability to flourish in the presence of the others in the sexually
recombining gene pool, is what creates the illusion of ‘unity of the geno-
type’. It is emphatically not right to say that because the genome is unified
in its embryological role, it is therefore also unified in its evolutionary role.
Mayr was right about embryology. Williams was right about evolution.
There is no disagreement.

DEDICATION
Dedicated, with the very deepest respect, to Professor Ernst Mayr FRS, Hon.
D. Sc (Oxford) on the occasion of his hundredth birthday.
52 / LUDUS VITALUS / vol. XII / num. 21 / 2004

REFERENCES
Crick F. H. C. (1958), “On protein synthesis,” in Symposium of the Society for
Experimental Biology XII. New York: Academic Press, p. 153.
Dawkins R. (1976), The Selfish Gene. Oxford: Oxford University Press.
Dawkins, R. (1982a), “Universal Darwinism,” in Bendall, E. (ed), Evolution from
Molecules to Men. Cambridge: Cambridge University Press.
Dawkins R. (1982b), The Extended Phenotype. Oxford: W.H Freeman and Com-
pany.
Dawkins R. (1998), Unweaving the Rainbow. London: Penguin Press.
Dennett D. (1995), Darwin’s Dangerous Idea. New York: Simon &Schuster
Hull D. L. (1980), “The units of evolution: A metaphysical essay,” in Jensen, U.L.
and R. Harre (eds.), Studies in the Concept of Evolution. Brighton: Harvester
Press.
Kimura, M. (1983), The Neutral Theory of Molecular Evolution. Cambridge: Cam-
bridge University Press.
Maynard Smith, J. (1982), Evolution and the Theory of Games. Cambridge: Cam-
bridge University Press.
Mayr, E. (1963), Animal Species and Evolution. Cambridge, Mass.: Harvard Uni-
versity Press.
Mayr, E. (1983), “How to carry out the adaptationist program?” American Natu-
ralist 121: 324-334.
Slobodkin, L. B. (1961), Growth and Regulation of Animal Populations. New York:
Holt, Rhinehart & Winston.
Sterelny, K. and Kitcher, P. (1988) “The return of the gene,” Journal of Philosophy
85: 339-361.
Tinbergen, N. (1963), “On aims and methods in ethology,” Zeitschrift für Tierp-
sychologie 20: 410-433.
Williams, G. C. (1966), Adaptation and Natural Selection. Princeton: Princeton
University Press.
Williams, G. C. (1992), Natural Selection: Domains, Levels and Challenges. Oxford:
Oxford University Press.
Wilson, E. O. (1992), The Diversity of Life. Cambridge, Mass.: Harvard University
Press.