Replicators and Vehicles
by Richard Dawkins
of natural selection provides a mechanistic, causal account of how living things
came to look as if they had been designed for a purpose. So overwhelming is the
appearance of purposeful design that, even in this Darwinian era when we know
"better," we still find it difficult, indeed boringly pedantic, to refrain from
teleological language when discussing adaptation. Birds' wings are obviously
"for" flying, spider webs are for catching insects, chlorophyll molecules are for
photosynthesis, DNA molecules are for. . . What are DNA molecules for?
The question takes us aback. In my case it touches off an almost audible alarm
siren in the mind. If we accept the view of life that I wish to espouse, it is the
forbidden question. DNA is not "for" anything. If we wish to speak teleologically,
all adaptations are for the preservation of DNA; DNA itself just is.
Following Williams (1966), I have advocated this view at length (Dawkins 1976,
1978), and I do not want to repeat myself here. Instead I shall try to clear up
an important misunderstanding of the view, a misunderstanding that has constituted
an unnecessary barrier to its acceptance.
The identity of the "unit of selection" has been controversial
in the literature both of biology (Williams, 1966; Lewontin, 1970; Leigh, 1977;
Dawkins, 1978; Alexander and Borgia, 1978; Alexander, 1980) and philosophy (Hull,
1981). In this paper I shall show that only part of the controversy is real. Part
is due to semantic confusion. If we overlook the semantic element, we arrive at a
simplistic hierarchical account of the views that have been expressed in the
literature. Living matter is nested in a hierarchy of levels, from ecosystem through
species, deme, family, individual, cell, gene, and even nucleotide base pair.
According to this analysis, each one of the protagonists in the debate on units of
selection is perched on a higher or a lower rung of a ladder, sniping at those
above and below him. Thus Gould (1977) remarks that in the last fifteen years:
challenges to Darwin's focus on individuals have
sparked some lively debates among evolutionists. These challenges have come from
above and from below. From above, Scottish biologist V. C. Wynne-Edwards raised
orthodox hackles fifteen years ago by arguing that groups, not individuals, are
units of selection, at least for the evolution of social behavior. From below,
English biologist Richard Dawkins has recently raised my hackles with his claim
that genes themselves are units of selection, and individuals merely their
At first blush, Gould's hierarchical analysis has a neatly
symmetrical plausibility. Much as my sense of mischief is tickled by the idea
of being allied with Professor Wynne-Edwards in a pincer-attack on Darwin's
individual however I reluctantly have to point out that the dispute between
individual and group is different in kind from the dispute between individual
and gene. Wynne-Edwards's attack from above is best seen as a factual dispute
about the level at which selection is most effective in nature. My attack from
below is a dispute about what we ought to mean when we talk about a unit of
selection. Much the same point has been realized by Hull (1981), but I prefer to
persist in expressing it in my way rather than to adopt his terminology of
"interactors" and "evolvors."
To make my point I shall develop a distinction between
replicator survival and vehicle selection. To anticipate the
conclusion: there are two ways in which we can characterize natural selection.
Both are correct; they simply focus on different aspects of the same process.
Evolution results from the differential survival of replicators. Genes
are replicators; organisms and groups of organisms are not replicators, they are
vehicles in which replicators travel about. Vehicle selection is the process by
which some vehicles are more successful than other vehicles in ensuring the
survival of their replicators. The controversy about group selection versus
individual selection is a controversy about whether, when we talk about a unit
of selection, we ought to mean a vehicle at all, or a replicator. In any
case, as I shall later argue, there may be little usefulness in talking about
discrete vehicles at all.
A replicator may be defined as any entity in the universe of
which copies are made. Replicators may be subclassified in two overlapping ways
(Dawkins, 1982, chapter 5). A germ-line replicator, as distinct from a dead-end
replicator, is the potential ancestor of an indefinitely long line of descendant
replicators. Thus DNA in a zygote is a germ-line replicator, while DNA in a liver
cell is a dead-end replicator. Cutting across this classification: an active, as
distinct from a passive, replicator is a replicator that has some causal influence
on its own probability of being propagated. Thus a gene that has phenotypic
expression is an active replicator. A length of DNA that is never transcribed and
has no phenotypic expression whatever is a passive replicator. "Selfish DNA"
(Dawkins, 1976, p. 47; Doolittle and Sapienza, 1980; Orgel and Crick, 1980), even
if it is not transcribed, should be considered passive only if its nature has
absolutely no influence on its probability of being replicated. It might be quite
hard to find a genuine example of a passive replicator. Special interest attaches
to active germ-line replicators, since adaptations "for" their preservation
are expected to fill the world and to characterize living organisms. Automatically,
those active germ-line replicators whose phenotypic effects happen to enhance their
own survival and propagation will be the ones that survive. Their phenotypic
consequences will be the attributes of living things that we see, and seek to
Active, germ-line replicators, then, are units of selection in
the following sense. When we say that an adaptation is "for the good of' something,
what is that something? Is it the species, the group, the individual, or what? I am
suggesting that the appropriate "something," the "unit of selection" in that sense,
is the active germ-line replicator. The active germ-line replicator might,
therefore, be called the "optimon," by extension of Benzer's (1957) classification
of genetic units (recon, muton, and cistron).
This does not mean, of course, that genes or other replicators
literally face the cutting edge of natural selection. It is their phenotypic effects
that are the proximal subjects of selection. I have been sorry to learn that the phrase
"replicator selection" can be misunderstood along those lines. One could, perhaps,
avoid this confusion by referring to replicator survival rather than replicator
selection. (In passing I cannot help being reminded of Wallace's (1866) passionate
plea to Darwin to abandon "natural selection" in favor of "survival of the fittest,"
on the grounds that many people thought "natural selection" implied a conscious
selecting "agent" (see also Young, 1971). My own prejudice is that anybody who
misunderstands "replicator selection" is likely to have even more trouble with
Natural selection does not inevitably follow whenever there exist
active germ-line replicators. Certain additional assumptions are necessary, but these,
in turn, are almost inevitable consequences of the basic definition. First, no copying
process is perfect, and we can expect that replicators will sometimes make inexact
copies of themselves, the mistakes or mutations being preserved in future descendants.
Natural selection, of course, depends on the variation so created. Second, the
resources needed to make copies, and to make vehicles for propagating copies, may be
presumed to be in limited supply, and replicators may therefore be regarded as in
competition with other replicators. In the complicatedly organized environments of
eukaryotic cells, each replicator is a competitor specifically of its alleles at its
own locus on the chromosomes of the population.
There is a problem over how large or how small a fragment of genome
we choose to regard as a replicator. Is it one cistron (recon, muton), one chromosome,
one genome, or some intermediate? The answer I have given before, and still stick by, is
that we do not need to give a straight answer to the question. Nobody is going to be
hanged as a result of our decision. Williams (1966) recognized this when he defined a
gene as "that which segregates and recombines with appreciable frequency" (p. 24), and
as "any hereditary information for which there is a favorable or unfavorable selection
bias equal to several or many times its rate of endogenous change" (p. 25). It is clear
that we are never going to sell this kind of definition to a generation brought up on
the "one geneone protein" doctrine, which is one reason why I (Dawkins, 1978) have
advocated using the word "replicator" itself, instead of "gene" in the sense of the
Williams definition. Another reason is that "replicator" is general enough to accommodate
the theoretical possibility, which one day may become observed reality, of nongenetic
natural selection. For example, it is at least worth discussing the possibility of
evolution by differential survival of cultural replicators or "memes" (Dawkins, 1976;
Bonner, 1980), brain structures whose "phenotypic" manifestation as behavior or artifact
is the basis of their selection.
I have lavished much rhetoric, or irresponsibly purple prose if you
prefer, on expounding the view that "the unit of selection" (I meant it in the sense
of replicator, not vehicle) must be a unit that is potentially immortal (Dawkins, 1976,
chapter 3), a point I learned from Williams (1966). Briefly, the rationale is that an
entity must have a low rate of spontaneous, endogenous change, if the selective
advantage of its phenotypic effects over those of rival ("allelic") entities is to
have any significant evolutionary effect. For a replicator such as a small length of
chromosome, mutation and crossing over within itself are hazards to its continued
replication, in exactly the same sense as are predators and reluctant females. Any
arbitrary length of DNA has an expected half-life measured in generations. The world
tends to become full of replicators with a long half-life, and therefore full of their
phenotypic products. These products are the characteristics of the animals and plants
we see around us. It is these that we wish to explain. Of those phenotypic products,
the ones that we, as whole animal biologists, are particularly interested in are those
that we see at the whole animal level, adaptations to avoid predators, to attract
females, to secure food economically, and so on. Replicators that tend to make the
successive bodies they inhabit good at avoiding predators, attracting females, etc.,
tend to have long half-lives as a consequence. But if such a replicator has a high
probability of internal self-destruction, through mutation in its broad sense, all
its virtues at the level or whole animal phenotypes come to naught.
It follows that although any arbitrary length of chromosome can in
theory be regarded as a replicator, too long a piece of chromosome will quantitatively
disqualify itself as a potential unit of selection, since it will run too high a risk
of being split by crossing over in any generation. A replicator worthy of the name,
then, is not necessarily as small as one recon, one muton, or one cistron. It is not
a discrete, all or none, unit at all, but a segment of chromosome whose length is
determined by the strength of the "whole animal level" selection pressure of interest.
As Francis Crick (1979) has written, "The theory of the 'selfish gene' will have to
be extended to any stretch of DNA."
It further follows that critics of the view advocated here cannot
score debating points by drawing attention to the existence of within-gene (cistron)
crossing over. I am grateful to Mark
Ridley for reminding me that most within-gene crossovers are, in any case,
indistinguishable in their effects from between-gene crossovers. Obviously, if the
gene concerned happens to be homozygous, paired at meiosis with an identical allele,
all the material exchanged will be identical, and the effect will be
indistinguishable from a crossover at either end of the gene. If the gene is
heterozygous, but differs from its allele by only one nucleotide, a within-gene
crossover will be indistinguishable in effect from a crossover at one of the two ends
of the gene. Only on the rare occasions when the gene differs from its allele in two
places, and the crossover occurs between the two places, will a within-gene
crossover be distinguishable from a between-gene crossover. The general point is
that it does not particularly matter where crossovers occur in relation to cistron
boundaries. What matters is where crossovers occur in relation to heterozygous
nucleotides. If, for instance, a sequence of six adjacent cistrons happens to be
homozygous throughout an entire species, a crossover anywhere within the six will be
exactly equivalent to a crossover at either end of the six.
The possibility of widespread linkage disequilibrium, too, does
not weaken the case (Clegg, 1978). It simply increases the length of chromosomal
segment that we expect to behave as a replicator. If (as seems doubtful) linkage
disequilibrium is so strong that populations contain "only a few gametic types"
(Lewontin, 1974, p. 312), the effective replicator will be a very large chunk of
DNA. When what Lewontin calls 1c the "characteristic
length" (the distance over
which coupling is effective), is only "a fraction of the chromosome length, each
gene is out of linkage equilibrium only with its neighbors but is assorted
essentially independently of other genes farther away. The characteristic length
is, in some sense, the unit of evolution since genes within it are highly correlated.
The concept is a subtle one, however. It does not mean that the genome is broken up
into discrete adjacent chunks of length 1c. Every locus is
the center of such a correlated segment and evolves in linkage with the genes near
it" (Lewontin, 1974, p. 312). In the same spirit, I played with the idea of
entitling an earlier work "The slightly selfish big bit of chromosome and the even
more selfish little bit of chromosome" (Dawkins, 1976, p.35).
I used to think that, in species with asexual reproduction, the
whole organism could be thought of as a replicator, but further reflection shows
this to be equivalent to the Lamarckian heresy. The asexual organism's genome
may be considered a replicator, since any alteration in it tends to be preserved.
But an alteration in the organism itself is quite likely to have been imprinted from
the environment and will not be preserved. It is not replicated. Asexual organisms
do not make copies of themselves, they work to make copies of their genomes.
An adaptation is a tool by which the genes that made it have
levered themselves through the past into the present, where it demands our
explanation. But the tools and levers do not rattle around loose in the world; they
come neatly packaged in tool kits: individual organisms or other vehicles. It is
to vehicles that we now turn.
Replicators are not naked genes, though they may have been when
life began. Nowadays, most of them are strung along chromosomes, chromosomes are
wrapped up in nuclear membranes, and nuclei are enveloped in cytoplasm and enclosed
in cell membranes. Cells, in turn, are cloned to form huge assemblages which we
know as organisms. Organisms are vehicles for replicators, survival machines as I
have called them. But just as we had a nested hierarchy of would-be
replicatorssmall and large fragments of genomeso there is a hierarchy
of nested vehicles. Chromosomes and cells are gene vehicles within organisms. In
many species organisms are not dispersed randomly but go around in groups.
Multispecies groups form communities or ecosystems. At any of these levels the
concept of vehicle is potentially applicable. Vehicle selection is the differential
success of vehicles in propagating the replicators that ride inside them. In theory
selection may occur at any level of the hierarchy.
One of the clearest discussions of the levels of selection is
that of Lewontin (1970), although his paper, like my own first discussion of the
matter (Dawkins, 1976), suffers from its failure to make a clear distinction
between replicators and vehicles. Lewontin does not mention the gene as one of
the levels in his hierarchy, presumably because he rightly regards it as obvious
that it is changes in gene frequency that ultimately matter, whatever level
selection may proximally act on. Thus it is easy, and probably largely correct,
to interpret his paper as being about levels of vehicle. On the other hand, at one
point he says the following:
The rate of evolution is limited by the variation in fitness of
the units being selected. This has two consequences from the point of view of
comparison between levels of selection. First, the rapidity of response to
selection depends upon the heritability of differences in fitness between units.
The heritability is highest in units where no internal adjustment or reassortment
is possible since such units will pass on to their descendent units an unchanged
set of information. Thus, cell organelles, haploid organisms, and gametes are
levels of selection with a higher heritability than diploid sexual genotypes,
since the latter do not perfectly reproduce themselves, but undergo segregation
and recombination in the course of their reproduction. In the same way,
individuals have a greater heritability than populations and assemblages of
species. (Lewontin, 1970, p. 8)
This point makes sense only if the units being referred to are
would-be replicators; indeed it is the same point I made a few pages back. This
suggests that Lewontin was not entirely clear over whether he was talking about
units of selection in the sense of replicators (entities that become more or less
numerous as a consequence of selection) or vehicles (units of phenotypic power of
replicators). The same is suggested by the fact that he cites M. B. Williams's
(1970) axiomatization of Darwin's theory as indicating that "the principles can
be applied equally to genes, organisms, populations, species, and at opposite
ends of the scale, prebiotic molecules and ecosystems." I would maintain that
genes and prebiotic molecules do not belong in the hierarchical list. They are
replicators; the rest are vehicles.
An organism is not a replicator, not even a very inefficient
replicator with a high probability of endogenous change. An organism's
genome can be regarded as a replicator (a very poor one if reproduction
is sexual), but to treat an organism as a replicator in the same sense as a gene
is tantamount to Lamarckism. If you change a replicator, the change will be
passed on to its descendants. This is clearly true of genes and genomes. It is
not true of organisms, since acquired characteristics are not inherited.
The reason we like to think in terms of vehicle selection is
that replicators are not directly visible to natural selection. Gould (1977, p.
24) put it well, albeit he mistakenly thought he was scoring a point against the
whole replicator concept: "I find a fatal flaw in Dawkins's attack from below.
No matter how much power Dawkins wishes to assign to genes, there is one thing
he cannot give them-direct visibility to natural selection. Selection simply
cannot see genes and pick among them directly. It must use bodies as an
intermediary." The valid point being made is that replicators do not expose
themselves naked to the world; they work via their phenotypic effects, and it is
often convenient to see those phenotypic effects as bundled together in vehicles
such as bodies.
It is another matter whether the individual body is the only
level of vehicle worth considering. That is what the whole group selection versus
individual selection debate is about. Gould comes down heavily in favor of the
individual organism, and this is the main one of the would-be units that I shall
Of all the levels in the hierarchy of vehicles, the
biologist's eye is drawn most strongly to the individual organism. Unlike the
cell and the population, the organism is often of a convenient size for the
naked eye to see. It is usually a discrete machine with an internally coherent
organization, displaying to a high degree the quality that Huxley (1912) labeled
"individuality" (literally indivisibility-being sufficiently heterogeneous in
form to be rendered nonfunctional if cut in half). Genetically speaking, too,
the individual organism is usually a clearly definable unit, each of whose
cells has the same genes as the others but different genes from the cells of
other individuals. To an immunologist, the organism has a special kind of
"uniqueness" (Medawar, 1957), in that it will easily accept grafts from other
parts of its own body but not from other bodies. To the ethologistand
this is really an aspect of Huxley's "individuality"the organism is a
unit of behavioral action in a much stronger sense than, say, half an organism,
or two organisms. The organism has one central nervous system. It takes
"decisions" (Dawkins and Dawkins, 1973) as a unit. All its limbs conspire
harmoniously together to achieve one end at a time. On occasions when two or
more organisms try to coordinate their efforts, say when a pride of lions
cooperatively stalks prey, the feats of coordination among individuals are
feeble compared with the intricate orchestration, with high spatial and
temporal precision, of the hundreds of muscles within each individual. Even a
starfish, each of whose tube-feet enjoys a measure of autonomy and may tear
the animal in two if the circum-oral nerve ring has been surgically cut, looks
like a single entity, and in nature behaves as if it had a single purpose.
For these and other reasons we automatically prefer to ask
functional questions at the level of the individual organism rather than at
any other level. We ask, "Of what use is that behavior pattern to the animal?"
We do not ask, "Of what use is the behavior of the animal's left hind leg to
the left hind leg?" Nor yet do we usually ask "Of what use is the behavior of
that pair of animals to the pair?" We see the single organism as a suitable
unit about which to speak of adaptation. No doubt this is why Hamilton
(1964a, b), in his epoch-making demonstration that individual altruism was
best explained as the result of gene selfishness, sugared the pill of his
scientific revolution by inventing "inclusive fitness"
as a sop to the individual organism. Inclusive fitness, in effect, amounts
to "that property of an individual organism which will appear to be maximized
when what is really being maximized is gene survival" (Dawkins, 1978). Every
consequence that Hamilton deduced from this theory could, I suggest, be
derived by posing the question: "What would a selfish gene do to maximize its
survival?" In effect, Hamilton was accepting the logic of gene (replicator)
selection while affirming his faith in the individual organism as the most
salient gene vehicle.
Presumably it would, in principle, be possible to imagine a
group-level equivalent of individual inclusive fitness: that property of a
group of organisms which will appear to be maximized when what is really
being maximized is the survival of the genes controlling the phenotypic
characters of the group. The difficulty with this is that, while we can
conceive of ways in which genes can exert phenotypic power over the limbs and
nervous systems of the bodies in which they sit, it is rather harder to
conceive of their exerting phenotypic power over the "limbs" and "nervous
systems" of whole groups of organisms. The group of organisms is too diffuse,
not coherent enough to be seen as a unit of phenotypic power.
And yet to some extent the individual organism, too, may be
not quite such a coherent unit of phenotypic power as we have grown to think.
It is certainly much less obviously so to a botanist than to a zoologist:
The individual fruit fly, flour beetle, rabbit,
flatworm or elephant is a population at the cellular but not at any higher
level. Starvation does not change the number of legs, hearts or livers of an
animal but the effect of stress on a plant is to alter both the rate of
formation of new leaves and the rate of death of old ones: a plant may react
to stress by varying the number of its parts. (Harper, 1977)
Harper feels obliged to coin two new terms for different
kinds of "individual." "The 'ramet' is the unit of clonal growth, the module
that may often follow an independent existence if severed from the parent
plant" (Harper, 1977, p. 24). The "genet," on the other hand, is the unit
that springs from one single-celled zygote, the "individual" in the normal
zoologists' sense. Janzen (1977) faces up to something like the same
difficulty, suggesting that a clone of dandelions should be regarded as
equivalent to a single tree, although spread out along the ground rather
than raised in the air, and divided up into separate physical "plants"
(Harper's ramets). Janzen sees a clone of aphids in the same way, although
Harper presumably would not: each aphid in a clone develops from a single
cell, albeit the cell is produced asexually. Harper would therefore say that
a new aphid is produced by an act of reproduction, whereas Janzen would
regard it as having grown like a new limb of its parent.
It might seem that we are now playing with words, but I
think Harper's (1977, p. 27) distinction between reproduction by means of a
single-celled (asexual or sexual) propagule, and growth by means of a
multicellular proppagule or runner, is an important one. What is more, it
can be made the basis of a sensible criterion for defining a single vehicle.
Each new vehicle comes into being through an act of reproduction. New parts
of vehicles come into being through growth. The distinction has nothing to
do with that between sexual and asexual reproduction, nor with that between
ramet and genet.
One Act of Reproduction, One Vehicle
I do not know whether Harper had the same thing in mind,
but for me the evolutionary significance of his distinction between growth
and reproduction is best seen as arising out of a view of development that
I learned from the works of J. T. Bonner (e.g., 1974). In order to make
complex adaptations at the level of multicellular organseyes, ears,
hearts, etc.a complex developmental process is necessary. An amoeba
may give rise to two daughters by splitting down the middle, but an eye, or
a heart, cannot give rise to two daughter eyes, or two daughter hearts, by
binary fission. Eyes and hearts are so complex that they have to be developed
from small beginnings, built by orderly cell division and differentiation.
This is why insects whose life cycle takes them through two radically
different bodies, like caterpillar and butterfly, do not attempt to
transform larval organs into corresponding adult organs. Instead, development
restarts from undifferentiated imaginal discs, the larval tissues being
broken down and used as the equivalent of food. Complexity can develop from
simplicity, but not from a wholly different kind of complexity. The
evolution of one complex organ into another can take place only because in
each generation the development of individuals restarts at a simple,
single-celled beginning (Dawkins, 1982, chapter 14).
Complex organisms all have a life cycle which begins with
a single cell, passes through a phase of mitotic cell division in which
great complexity of structure may be built up, and culminates in reproduction
of new single-celled propagules of the next generation. Evolutionary change
consists in genetic changes which alter the developmental process at some
crucial stage in the life cycle, in such a way that the complex structure of
the organism of the next generation is different. If organisms simply grew
indefinitely, without returning cyclically to a single-celled zygote in a
sequence of generations, the evolution of complexity at the multicellular
organ level would be impossible. For lineages to evolve, individuals must
develop from small beginnings in each generation. They cannot just grow from
the multicellular bodies of the previous generation.
We must beware of falling into the trap of "biotic
adaptationism" here (Williams, 1966). We cannot argue that a tendency to
reproduce rather than grow will evolve in order to allow evolution to happen!
Rather, when we look at complex living things we are looking at the end
products of an evolutionary process which could only occur because the
lineages concerned showed repeated reproduction rather than just growth. A
related point is that reepeated cycles of reproduction are only possible if
there is also death of individual vehicles, but this is not, in itself, a
reason that explains why death occurs. We cannot say that the biological
function of death is "to" allow reepeated reproduction, hence evolution
(Medawar, 1957). But given that death and reproduction do occur in a lineage,
evolution in that lineage becomes possible (Maynard Smith, 1969).
Is the distinction between growth and reproduction a rigid
one? As so far defined it seems so. A life cycle that restarts with a single
cell represents a new reproductive unit, a new discrete vehicle. All other
apparent reproduction should be called growth. But couldn't there be a new
life cycle that was initiated not by a single-celled propagule but by a small
multicellular proppagule? When a new plant grows from a runner sent out by an
old plant, is this reproduction or growth? If Harper's definition is rigidly
applied, everything depends on an embryological detail. Are all the cells of
the new "plant" the clonal descendants of one cell at the growing tip of the
runner? In this case we are dealing with reproduction. Or is the runner a
broad-fronted meristem, so that some cells in the new plant are descended from
one cell in the old plant, while other cells in the new plant are descended
from another cell in the old plant? In this case the Harper definition forces
us to classify the phenomenon as growth, not reproduction. It is, in
principle, not different from the growth of a new leaf on a tree.
That is what follows from the Harper definition, but is it
a sensible definition? I can think of one good reason for saying yes. It makes
sense if we are regarding reproduction as the process by which a new vehicle
comes into existence, and growth as the process by which an existing vehicle
develops. Imagine a plant that sends out vegetative suckers that are
broad-fronted meristems, and suppose that this species never reproduces
sexually. How might evolutionary change occur? By mutation and selection in
the usual way, but not by selection among multicellular organisms. A mutation
would affect the cell in which it occurred, and all clonal descendants of that
cell. But because the runner is broad-fronted, new "plants" (ramets) would be
heterogeneous mosaics with respect to the mutation. Some of the cells of a new
plant would be mutant, others would not. As the vegetation creeps over the
land, mutant cells are peppered in haphazard bunches around the "individual"
plants. The apparent individual plants, in fact, are not genetic individuals
at all. Since they are genetic mosaics, the largest gene vehicle that can be
discerned as having a regular life cycle is the cell. Population genetics
would have to be done at the cellular level, not at the "individual" level.
And vehicle selection would give rise to adaptive modification at the cellular
level, but not at the level of the whole "plant." The whole "plant" would not
function as a vehicle propagating the genes inside it, because different cells
inside it would contain different genes. Cells would function as vehicles, and
adaptations would not be for the good of the whole plant but for the good of
smaller units within the plant. To qualify as a "vehicle," an entity must come
into being by reproduction, not by growth.
That is my justification for the importance of the Harper
definition. But now suppose that the runner is a narrow bottleneck of mitotic
cell descent, so that the life cycle consists of an alternation between a
growth phase and a small, if multicellular, restarting phase. "Individual
plants" would now be statistically unlikely to be genetic mosaics. In this
case vehicle selection at the level of whole plants could go on, in a
statistical sense, since most, though not all, plants would be genetically
uniform. Genetic variation within the cells of individual plants would be
less than that between cells of different plants. A kind of "group selection"
(J. Hartung, personal communication) at the cellular level could therefore go
on, leading to adaptation at the level of the multicellular vehicle, the
level of the "individual plant." We might therefore tolerate a slight
relaxation of Harper's criterion, using "reproduction" whenever a life cycle
is constricted into a narrow bottleneck of cells, even if that bottleneck is
not always quite as narrow as a single cell.
We are now, incidentally, in a position to see a reason,
additional to those normally given, why the individual organism is so much
more persuasive a unit of natural selection (vehicle) than the group of
organisms. Groups do not go through a regular cycle of growth (development),
alternating with "reproduction" (sending off a small "propagule" which
eventually grows into a new group). Groups grow in a vague and diffuse
manner, occasionally fragmenting like pack ice. It is significant that
models of group selection that come closest to succeeding tend to incorporate
some reproduction-like process. Thus Levins, and Boorman and Levitt (reviewed
by Wilson, 1973) postulate a metapopulation of groups, in which populations
"reproduce" by sending out "propagules" consisting of migrant individuals or
small bands of individuals. Moreover, "group selection" in the sense of D. S.
Wilson (1980) can only work if there is some mechanism by which genetic
variation between groups is kept higher than genetic variation within groups
(Maynard Smith, 1976; Grafen, 1980, and in preparation). This point is
analogous to the one I made in my discussion of "cellular selection" in
plants with narrow runners. In practice the most likely way for intergroup
variation to be higher than intragroup variation is through genetic
relatives tending to associate together. In this case we are dealing with
what has been called kin-group selection. Is "kin selection," then, an
authentic case where we have a vehicle larger than the individual body, in
the same way group selection would be if it existed?
Kin Selection and Kin Group Selection
There are those who see kin selection as a special case of
group selection (E. O. Wilson, 1973; D.S. Wilson, 1980; Wade, 1978). Maynard
Smith (1976) disagrees, and emphatically so do I (Dawkins, 1976, 1978, 1979).
Maynard Smith is too polite in suggesting that the disagreement is merely
one between lumpers and splitters. Hamilton (1975) at first reading might be
thought to be endorsing the lumping of kin and group selection. To avoid
confusion I quote him in full:
If we insist that group selection is different
from kin selection the term should be restricted to situations of assortation
definitely not involving kin. But it seems on the whole preferable to retain
a more flexible use of terms; to use group selection where groups are clearly
in evidence and to qualify with mention of "kin" (as in the "kin-group"
selection referred to by Brown, 1974). (Hamilton, 1975, p. 141, citation of
Hamilton is here making the distinction between kin
selection and kin-group selection. Kin-group selection is the special case of
group selection in which individuals tend to be closely related to other
members of their own group. It is also the special case of kin selection in
which the related individuals happen to go about in discrete family groups.
The important point is that the theory of kin selection does not need to
assume discrete family groups. All that is needed is that close relatives
encounter one another with higher than random frequency, or have some method
of recognizing each other (Maynard Smith, 1982). As Hamilton says, the term
"kin selection" (rather than "kin-group selection") "appeals most where
pedigrees are unbounded and interwoven."
I have previously quoted Hull (1976) on mammary glands:
"mammary glands contribute to individual fitness, the individual in this
case being the kinship group." Hull is here using "individual" in a special,
philosopher's sense, as "any spatio-temporally localized, cohesive and
continuous entity." In this sense "organism" is not synonymous with
"individual" but is only one of the class of things that can be called
individuals. Thus Ghiselin (1974) has argued that species are "individuals."
The point I wish to make here is that the "kinship group" is an "individual"
only if families go about in tightly concentrated bands, rigidly
discriminating family members from nonmembers, with no half measures.
There is no particular reason for expecting this kind of rigid family
structure in nature, and certainly Hamilton's theory of kin selection
does not demand it. As I suggested when I originally quoted Hull (Dawkins,
1978), we are not dealing with a discrete family group but with an animal
plus 1/2 of each of its children plus 1/2 of each sibling plus 1/4 of each
niece and grandchild plus 1/8 of each first cousin plus ·1/32 of each second
cousin . . . Far from being a tidy, discrete group, it is more like a sort
of genetical octopus, a probabilistic amoeboid whose pseudopodia ramify and
dissolve away into the common gene pool.
Where they exist, tightly knit family bands, or "kin
groups," may be regarded as vehicles. But the general theory of kin selection
does not depend on the existence of discrete family groups. No vehicle above
the organism level need be postulated.
Doing Without Discrete Vehicles
It will have been noted that my "vehicles" are
"individuals" in the sense of Ghiselin and Hull. They are spatiotemporally
localized, cohesive, and continuous entities. Much of my section on
organisms was devoted to illustrating the sense in which bodies, unlike
groups of bodies, are "individuals." My sections on vegetatively
propagating plants and on kin groups suggested that while they sometimes
may be discrete and cohesive entities, there is no reason, either
in fact or in theory, for expecting that they usually will be so. Kin
selection, as a logical deduction from fundamental replicator theory,
still leads to interesting and intelligible adaptation, even if there are
not discrete kin-group vehicles.
I now want to generalize this lesson: although selection
sometimes chooses replicators by virtue of their effects on discrete
vehicles, it does not have to. Let me repeat part of my quotation from
Gould (1977): "Selection simply cannot see genes and pick among them
directly. It must use bodies as an intermediary." Well, it must use
phenotypic effects as intermediaries, but do these have to be bodies?
Do they have to be discrete vehicles at all? I have suggested (Dawkins, 1982)
that we should no longer think of the phenotypic expression of a gene as
being limited to the particular body in which the gene sits. We are already
accustomed to the idea of a snail shell as phenotypic expression of genes,
even though the shell does not consist of living cells. The form and color
of the shell vary under genetic control. In principle the same is true of a
caddis larva's house, though in this case building behavior intervenes in
the causal chain from genes to house. There is no reason why we should not
perform a genetic study of caddis houses, and a question such as "Are
round stones dominant to angular stones?" could be a perfectly sensible
research question. A bird's nest and a beaver dam are also extended
phenotypes. We could do a genetic study of bower bird bowers in exactly the
same sense as a genetic study of bird of paradise tails. I continue this
conceptual progression further in the book referred to, concluding that
genes in one body may have phenotypic expression in another body. For
instance, I argue that genes in cuckoos have phenotypic expression in host
behavior. When we look at an animal behaving, we may have to learn to say,
not "How is it benefiting its inclusive fitness?" but rather "Whose
inclusive fitness is it benefiting?"
Gould is right that genes are not naked to the world.
They are chosen by virtue of their phenotypic consequences. But these
phenotypic consequences should not be regarded as limited to the particular
individual body in which the gene sits, any more than traditionally they
have been seen as limited to the particular cell in which the gene sits
(red blood corpuscles and sperm cells develop under the influence of genes
that are not inside them). Not only is it unnecessary for us to regard the
phenotypic expression of a gene as limited to the body in which it sits.
It does not have to be limited to any of the discrete vehicles it can be
described as inhabitingcell, organism, group, community, etc. The
concept of the discrete vehicle may turn out to be superfluous. In this
respect, if I understand him aright, I am very encouraged by Bateson (1982,
p. 136) when he says, "Insistence on character selection and nothing else
does not commit anyone to considering just the attributes of individual
organisms. The characters could be properties of symbionts such as
competing lichens or mutualistic groups such as competing bands of wolves."
However, I think Bateson could have gone further. The use of the word
"competing" in the last sentence quoted suggests that he remains somewhat
wedded to the idea of discrete vehicles. An entity such as a band of
wolves must be a relatively discrete vehicle if it is to be said to
compete with other bands of wolves.
I see the world as populated by competing replicators
in germ lines. Each replicator, when compared with its alleles, can be
thought of as being attached to a suite of characters, outward and visible
tokens of itself. These tokens are its phenotypic consequences, in
comparison with its alleles, upon the world. They determine its success or
failure in continuing to exist. To a large extent the part of the world a
gene can influence may happen to be limited to a local area that is
sufficiently clearly bounded to be called a body, or some other discrete
vehicleperhaps a wolf pack. But this is not necessarily so. Some of
the phenotypic consequences of a replicator, when compared with its
alleles, may reach across vehicle boundaries. We may have to face the
complexity of regarding the biosphere as an intricate network of
overlapping fields of phenotypic power. Any particular phenotypic
characteristic will have to be seen as the joint product of replicators
whose influence converges from many different sources, many different
bodies belonging to different species, phyla, and kingdoms. This is the
doctrine of the "extended phenotype."
In the present paper I have mainly tried to clear up a
misunderstanding. I have tried to show that the theory of replicators,
which I have previously advocated, is not incompatible with orthodox
"individual selectionism." The confusion over "units of selection" has
arisen because we have failed to distinguish between two distinct
meanings of the phrase. In one sense of the term "unit," the unit that
actually survives or fails to survive, nobody could seriously claim that
either an individual organism or a group of organisms was a unit of
selection; in this sense the unit has to be a replicator, which will
normally be a small fragment of genome. In the other sense of unit, the
"vehicle," either an individual organism or a group could be a serious
contender for the title "unit of selection." There are reasons for
coming down on the side of the individual organism rather than larger
units, but it has not been a main purpose of this paper to advocate this
view. My main concern has been to emphasize that, whatever the outcome of
the debate about organism versus group as vehicle, neither the organism
nor the group is a replicator. Controversy may exist about rival candidates
for replicators and about rival candidates for vehicles, but there should
be no controversy over replicators versus vehicles. Replicator survival
and vehicle selection are two aspects of the same process. The first
essential is to distinguish clearly between them. Having done so, we may
argue the merits of the rival candidates for each, and we may go on to ask,
as I briefly did at the end, whether we really need the concept of
discrete vehicles at all. If the answer to this turns out to be no, the
phrase "individual selection" may be misleading. Whatever the upshot of
the latter debate about the extended phenotype, I hope here to have removed
an unnecessary source of semantic confusion by exposing the difference
between replicators and vehicles.
(1) The question of "units of selection" is not trivial.
If we are to talk about adaptations, we need to know which entity in the
hierarchy of life they are "good" for. Adaptations for the good of the group
would look quite different from adaptations for the good of the individual or
the good of the gene.
(2) At first sight, it appears that "the individual" is
intermediate in some nested hierarchy between the group and the gene. This
paper shows, however, that the argument over "group selection" versus
"individual selection" is a different kind of argument from that between
"individual selection" and "gene selection." The latter is really an argument
about what we ought to mean by a unit of selection, a "replicator" or a
(3) A replicator is defined as any entity in the universe
of which copies are made. A DNA molecule is a good example. Replicators are
classified into active (having some "phenotypic" effect on the world which
influences the replicator's chance of being copied) and passive. Cutting
across this they are classified into germ-line (potential ancestor of an
indefinitely long line of descendant replicators) and dead-end (e.g., a gene
in a liver cell).
(4) Active, germ-line replicators are important. Wherever
they arise in the universe, we may expect some form of natural selection and
hence evolution to follow.
(5) The title of "replicator" should not be limited to any
particular chunk of DNA such as a cistron. Any length of DNA can be treated
as a replicator, but with quantitative reservations depending on its length,
on recombination rates, linkage disequilibrium, selection pressures, etc.
(6) An individual organism is not a replicator, because
alterations in it are not passed on to subsequent generations. Where
reproduction is asexual, it is possible to regard an individual's whole
genome as a replicator, but not the individual itself.
(7) Genetic replicators are selected not directly but by
proxy, via their phenotypic effects. In practice, most of these phenotypic
effects are bundled together with those of other genes in discrete
"vehicles"individual bodies. An individual body is not a replicator;
it is a vehicle containing replicators, and it tends to work for the
replicators inside it.
(8) Because of its discreteness and unitariness of
structure and function, we commonly phrase our discussions of adaptation at
the level of the individual vehicle. We treat adaptations as though they were
"for the good of' the individual, rather than for the good of some smaller
unit like a single limb, or some more inclusive vehicle such as a group or
(9) But even the individual organism may be less unitary
and discrete than is sometimes supposed. This is especially true of plants,
where it seems to be necessary to define two different kinds of
"individuals""ramets" and "genets."
(10) An individual may be defined as a unit of
reproduction, as distinct from growth. The distinction between
reproduction and growth is not an easy one, and it should not be confused
with the distinction between sexual and asexual reproduction. Reproduction
involves starting anew from a single-celled propagule, while growth
(including vegetative "reproduction") involves "broad-fronted" multicellular
(11) Kin selection is quite different from group selection,
since it does not need to assume the existence of kin groups as discrete
vehicles. More generally, we can question the usefulness of talking about
discrete vehicles at all. In some ways a more powerful way of thinking is in
terms of replicators with extended phenotypes in the outside world,
effects which may be confirmed within the borders of discrete vehicles but do
not have to be.
(12) The concept of the discrete vehicle is useful,
however, in clarifying past discussions. The debate between "individual
selection" and "group selection" is a debate over rival vehicles. There
really should be no debate over "gene selection" versus "individual (or group)
selection," since in the one case we are talking about replicators, in the
other about vehicles. Replicator survival and vehicle selection are two views
of the same process. They are not rival theories.
I have benefited from discussion with Mark Ridley, Alan
Grafen, Marian Dawkins, and Pat Bateson and other members of the conference
at King's College. Some of the arguments given here are incorporated, in
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[ Richard Dawkins, "Replicators and Vehicles," King's College
Sociobiology Group, eds., Current
Problems in Sociobiology, Cambridge, Cambridge University Press, (1982), pp. 45-64;
Reprinted here from Robert Brandon and Richard Burian, Genes, Organisms, Populations,
Cambridge MA, The MIT Press, 161-180. ]
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