Toward a Modern Revival of Darwins Theory of Evolutionary Novelty


Toward a Modern Revival of Darwin’s Theory of Evolutionary Novelty
Author(s): Mary Jane West‐Eberhard
Reviewed work(s):
Source: Philosophy of Science, Vol. 75, No. 5, Proceedings of the 2006 Biennial Meeting of the
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Philosophy of Science, 75 (December 2008) pp. 899–908. 0031-8248/2008/7505-0034$10.00
Copyright 2008 by the Philosophy of Science Association. All rights reserved.

899

Toward a Modern Revival of Darwin’s
Theory of Evolutionary Novelty

Mary Jane West-Eberhard†‡

Darwin proposed that evolutionary novelties are environmentally induced in organisms
“constitutionally” sensitive to environmental change, with selection effective owing to
the inheritance of constitutional responses. A molecular theory of inheritance, pan-
genesis, explained the cross-generational transmission of environmentally induced
traits, as required for evolution by natural selection. The twentieth-century evolutionary
synthesis featured mutation as the source of novelty, neglecting the role of environ-
mental induction. But current knowledge of environmentally sensitive gene expression,
combined with the idea of genetic accommodation of mutationally and environmentally
induced change, supports a revival of Darwin’s original theory that is consistent with
modern molecular and population genetics.

1. Introduction. An evolutionary novelty can be defined as a discrete phe-
notypic trait that is new in composition or context of expression relative to
established ancestral traits (see, e.g., West-Eberhard 2003; Hall 2005; Kap-
lan 2007). In this essay, I will consider novelties that are somewhat com-
plex—the kind of phenotypic traits that Darwin attempted to explain as
products of selection and gradual change. And I will include the estab-
lishment of novelties in populations or lineages as regularly occurring
traits, not just their initial appearance. The initial appearance of a novelty
is an event that depends on preexisting developmental capacities used in
other aspects of development, or on “latent capacities” that become evi-
dent (reawakened or newly assembled) when a novelty is initially evoked
(Hall 2005). I will consider only the evolution of adaptive novelties—that

†To contact the author, please write to: Smithsonian Tropical Research Institute, c/o
Escuela de Biologı́a, Universidad de Costa Rica, Costa Rica; e-mail: mjwe@sent.com.

‡This essay is based on “Darwin’s Argument and Controversy regarding the Causes
of Evolutionary Innovation,” a paper presented at the annual symposium of the Phi-
losophy of Science Association, Vancouver, BC, November 2006. I thank Jonathan
Kaplan and Massimo Pigliucci for the invitation to participate in that symposium, “Evo-
lutionary Innovation and Novelties,” and William G. Eberhard for helpful suggestions.



900 MARY JANE WEST-EBERHARD

is, Darwinian evolution by natural selection. I will not consider pre-Dar-
winian or non-Darwinian explanations.

2. Darwin’s Theory as a Causal Chain to Explain Adaptive Evolution. A
satisfactory theory of novelty has to have a series of explanatory elements
lined up in what might be called a “causal chain,” with a satisfactory
mechanism for each step. As outlined by Darwin, the evolution of an
adaptive novelty under natural selection is a two-step process: first var-
iation, then spread. Beginning with an ancestral population, such a theory
has to describe two aspects of variation: its inception—the initiation of
change (the new input that gets it started—an upstream, stimulatory, or
regulatory event); and the origin of new form—where the phenotypic end
product comes from. Then, to account for spread in Darwinian terms,
there has to be an explanation for how the novel variant affects selection
(differential reproductive success), which causes an increase in frequency
of the novelty within a population. But selection alone is not enough to
explain evolution, because it does not explain cumulative phenotype-fre-
quency change that continues across many generations. Such cross-gen-
erational change requires inheritance of the trait, which, together with
selection, produces a change in frequency over time (adaptive evolution).
Differential reproduction without inheritance of the fitness-affecting trait
variation, as could occur between differently nourished members of a
clone, produces only short-term change in phenotype frequencies.

Darwin’s theory of novelty is a marvelously complete and ingenious
analysis of this causal chain. In describing it, I will translate partially into
modern terms for the sake of clarity and brevity. According to Darwin,
the initiation of change is often associated with changed conditions ([1859]
1872, 15–16). The new conditions cause increased variability, including
small discrete novel variants, which Darwin called “individual differences”
or “pecularities.” These, he observed, can be small, medium, or large—
even “monstrous”—in size ([1859] 1872, 38–39). The variation can be due
to direct effects of the new conditions on the preexisting phenotypes (as
in the use and disuse of limbs). But Darwin considered newly induced
variations to be influenced significantly by the nature of the organism
itself, or what Darwin called “constitutional” properties: “Organic beings,
when subjected during several generations to any change whatever in their
conditions, tend to vary; the kind of variation that ensues depending in
most cases in a far higher degree on the nature or constitution of the
being, than on the nature of the changed conditions” ([1868] 1972, 237).
In other words, Darwin observed that variation generated in response to
conditions depends on what we would now call the genetically influenced
makeup of the individual phenotype.

Given an array of newly induced variations, individuals showing dif-



MODERN THEORY OF EVOLUTIONARY NOVELTY 901

ferent degrees of development of a novel trait will exhibit different degrees
of survival or success in reproduction (natural or sexual selection; Darwin
[1859] 1872). But the problem of identifying a mechanism for inheritance
remained to be solved. If a novelty is originally environmentally induced,
how can natural selection increase that novelty’s predominance in a pop-
ulation over time? Even if the conditional responses are seen as being to
some degree inherited, or “constitutional,” from their initiation, the re-
sponse is still dependent upon conditions. How can there be a lasting effect
on the constitutional properties of individuals to explain the observed in-
crease in the frequency of environmentally induced traits?

Once the material basis for inheritance was known to be the gene, the
spread of genetically influenced conditional phenotypes could be identified
with the spread of genes. This would have followed easily from Darwin’s
observation (discussed above) that variation in the response to conditions
depends significantly on variation in constitution. But Darwin could not
make the connection between conditional expression and genetic inheri-
tance the way we can make it today nor could he have solved the problems
of inheritance he observed had he known about Mendel’s work,1 which
did not explain the inheritance of condition-sensitive or of quantitatively
variable traits.

Darwin reasoned clearly that an increase in the commonness of an
environmentally induced trait would have to depend on inheritance, not
on the environmental factor itself: “A fancier who wished to decrease the
size of his bantams or tumbler-pigeons would never think of starving them,
but would select the smallest individuals which spontaneously appeared.
. . . Although every variation is either directly or indirectly caused by some
change in the surrounding conditions, we must never forget that the nature
of the organization which is acted on, is by far the more important factor
in the result” ([1868] 1972, 415).

To solve the problem of the inheritance of environmentally induced
novelties under positive selection, Darwin invented a molecular theory of
the gene—his theory of pangenesis (see esp. [1868] 1972). He hypothesized
the existence of tiny particles, which he called “gemmules,” that accu-
mulate over generations of positive selection in the region of the body
where a novelty is expressed. These particles could then be transmitted
between generations. Darwin realized—and this is something that is often
forgotten, for it was a feature of genetics ignored by the twentieth-century
synthesis—that inheritance involves both the transmission and the ex-
pression of traits; the molecular gemmules, like DNA, were the material

1. Despite Darwin’s considerable research and correspondence as a plant breeder (see
esp. [1868] 1972), including extensive work on peas, there is now virtually no doubt
that he was not aware of Mendel’s work (Sclater 2003).



902 MARY JANE WEST-EBERHARD

basis for both. Only now, when the age of Mendelian transmission genetics
has given way to the age of gene expression, are we beginning to ade-
quately appreciate this twofold role of the genome in both the transmission
and the expression of phenotypic traits.

In sum, Darwin explained the increased inheritance of acquired traits
with a kind of “genetic assimilation,” erroneously ascribed to phenotyp-
ically local effects on the particles of inheritance under natural selection.
Darwin had to imagine a purely hypothetical mechanism to account for
the observed and reported facts because in the late 1800s he had no other
choice. He was completely aware of the limitations of his speculations in
these respects: he termed his hypothesis of pangenesis “provisional” and
acknowledged that it was subject to “a certain portion of incompleteness,
and even of error” ([1868] 1972, 349–350). And he repeatedly mentioned
the inadequacy of contemporary understanding of the causes of variation:
“At the present time there is hardly any question in biology of more
importance than this of the nature and causes of variability” (1882, vi).

The claim by some (e.g., Pinker 1998, 522) that “Darwin’s . . . embrace
of Larmarckism . . . was perhaps his biggest scientific blunder” seems
unfair when one considers Darwin’s caution regarding his speculations
on the mechanism of inheritance, the tendency in subsequent discussions
(including those taking place during the twentieth-century synthesis) to
brush aside observations that Darwin considered of major importance
(the eventual inheritance of environmentally altered phenotypes), and
Darwin’s seeming ambivalence regarding the inheritance of acquired
traits. On the one hand, his highly tentative theory of pangenesis was
Lamarckian (and erroneous) in hypothesizing that use could alter the
material of inheritance. On the other hand, his discussion of inheritance
was sometimes explicitly dismissive of Larmarck: upon noting that social
insect workers (which do not reproduce) have traits passed on via the
reproduction of queens (which do not work), Darwin concluded, “I am
surprised that no one has hitherto advanced this demonstrative case of
neuter insects, against the well-known doctrine of inherited habit, as ad-
vanced by Lamarck” ([1859] 1872, 207). Much of Darwin’s discussion
([1859] 1872, [1868] 1972) of “direct and definite action of the external
conditions of life” and on “use and disuse” refers not to Lamarckian
inheritance but to what we would now call “phenotypic plasticity.”

Finally, Darwin placed enormous emphasis on the importance of cu-
mulative gradualism to explain the origin of complexity. In fact, he staked
his whole argument on the principle of gradual change and asserted that
the whole theory of evolution by natural selection could be falsified if
any exception could be found. He wrote: “If it could be demonstrated
that any complex organ existed, which could not possibly have been
formed by numerous, successive, slight modifications, my theory would



MODERN THEORY OF EVOLUTIONARY NOVELTY 903

absolutely break down” ([1859] 1872, 135). It is worth noting that with
this statement, and others like it, Darwin’s theory meets the scientific
requirement of falsifiability.

In that passage of his writing, Darwin places great emphasis on grad-
ualism, when at the same time he stated that novel variants could be large
and even “monstrous” in size. Isn’t this a contradiction? It would seem
that the existence of monstrous selectable variants would make his theory
absolutely break down. Although Darwin recognized the existence of large
variants, he consistently downplayed their importance. He did so in order
to emphasize the central importance of selection. If he had given too
much credit to variation, that would have detracted from the power of
selection and would, in turn, have opened the door to the possibility of
saltatory developmental origins, or even divine creation, of complex novel
design. But Darwin had a clever way to remove this contradiction between
gradualism and the occurrence of large developmental variants, which I
call retrospective gradualism: he argued that some saltatory phenomena
such as heterochrony and one-step reversions were simply the altered
expressions of traits that had evolved gradually in the past. In other words,
complex reorganizational variants are not really novelties—they are just
old products of gradual evolution whose timing of expression has changed.

3. Mendelian Genetics: A Mutation-Based Incomplete Causal Chain. Peo-
ple are fond of saying that Mendelian genetics solved the problem of
inheritance that Darwin had failed to understand. But Mendelian genetics
did not account for all of the facts of inheritance that Darwin had ob-
served. The version of evolutionary theory inspired by Mendelian ge-
netics—the “synthesis” of mid-twentieth-century evolutionary biology—
was in some respects oversimplified and incomplete. The mutation-based
causal chain for the origin of novelty was depicted as follows (see Huxley
1942, 51): a genetic mutation leads (by an undescribed mechanism) to the
production of a small phenotypic change in a single individual. Then,
owing to a fitness increase associated with the mutant genetic allele, the
mutant gene and the associated phenotype increase in the population over
subsequent generations. A complex novelty requires a series of mutations.
The problem of inheritance is solved by the cross-generational transmis-
sion of genetic alleles that have a one-to-one correspondence to the se-
lected phenotype. This scheme was an incomplete account of the phe-
nomena to be explained:

• There is no role for environmental induction—even though the en-
vironmental induction of developmental variants is an obvious and
undeniable fact, as extensively documented by Darwin and many
studies since.



904 MARY JANE WEST-EBERHARD

• The mechanism for an effect of mutation on trait development is a
black box.

• And any hint that large developmental variants could play a role in
evolution is strongly rejected (by, e.g., Fisher 1930; Charlesworth,
Lande, and Slatkin 1982), even though such variants occur and
evidently can become established during evolution (see West-Eber-
hard 2003, Chapters 9–19, on evolution by developmental reorgan-
ization of the phenotype, sometimes gradual, sometimes by large
steps). No hopeful monsters or macromutations are allowed. This
synthesis is a strict version of gradualism, in some respects more
uncompromising than Darwin’s. It followed Darwin in emphasizing
the importance of selection, and it went further than Darwin in the
corresponding de-emphasis of developmental causes of variation.

In some respects, this is an evolutionary theory in denial, conceptually
blind to the environmental sensitivity of phenotypes and to the fact that
selection, which acts on phenotypes, must necessarily act on environ-
mentally induced variation as well as on mutationally induced change.

This is a caricature, of course, and there were exceptions. C. H. Wad-
dington was one of them—others were Baldwin (1896, 1902) and Schmal-
hausen ([1949] 1986), but their ideas were less explicitly related to genetics
than were Waddington’s. Waddington did figure out a way, through his
concept of “genetic assimilation” (1953), to incorporate environmental
induction into the genetic theory. Genetic assimilation treated environ-
mentally induced traits as polygenic threshold traits, which could spread
if positive selection lowered the threshold for their expression.

Even if this idea had been incorporated into the twentieth-century syn-
thesis, which it was not (for various interesting reasons; see West-Eberhard
2003, 415–416), Waddington’s genetic assimilation did not really complete
the synthesis as an explanation of novelties. In Section 4, I outline an
expanded, remedial proposal.

4. The Origin of Novelty: A Modern Darwinian Causal Chain.

4.1. Phases in the Origin and Evolution of a Novel Trait. I propose that
we consider a causal chain that builds on Waddington’s insights, as well
as on those of the twentieth-century synthesis, but is more complete—more
like Darwin’s but taking advantage of what we now know about the mo-
lecular basis of inheritance and trait expression.

As in Darwin’s theory, innovation begins with a population of consti-
tutionally (genetically and phenotypically) variable environmentally sen-
sitive organisms. Then a novel input or initiator impinges on some in-
dividuals. The novel input can be either a mutation or an environmental
change, such as the uptake of a new building block from outside the



MODERN THEORY OF EVOLUTIONARY NOVELTY 905

organism, or a new environmental stimulus whose effect is mutation-like
in that it induces some novel developmental response. The initiator in-
teracts with the existing, genetically variable individuals, which then react
to it with purely phenotypic adjustments (phenotypic accommodation).
Some are more responsive than others, and they respond in somewhat
different ways to produce a population of individuals possessing the novel
phenotype. From the beginning, the novel phenotype would be variable
both in its form and in the threshold for its production, due in part to
the preexisting genetic variation in the responding population. Then pos-
itive or negative selection can produce the genetic accommodation of the
trait. Genetic accommodation (West-Eberhard 2003) is just gene frequency
change due to selection on the genetically variable regulation and form
of a novel trait, or of a trait undergoing selection in altered (new) cir-
cumstances. Genetic accommodation does not require mutation. It de-
pends on the existence of a standing crop of genetic variation in the
population under selection. That such genetic variation exists for virtually
all traits is supported by research on genetic polymorphisms and selection
experiments using populations of wild and domesticated organisms
(Schmalhausen [1949] 1986; reviews in West-Eberhard 2003; Kaplan
2007).

Note that in this scheme much phenotypic change can take place before
there is any appreciable gene-frequency change, due to phenotypic ac-
commodation (West-Eberhard 2003), which can be an adaptively appro-
priate phenotypic adjustment and can involve extensive remodeling of
development. Even if a novelty begins with a mutation, most of the genetic
change affecting its spread would usually come later, in the form of genetic
accommodation.

4.2. Genetic Accommodation and Genetic Assimilation Compared. Ge-
netic accommodation allows for a more complete description of genetic
change during the evolution of novelty than that suggested by the idea
of genetic assimilation, which depicts all change as moving toward in-
creased frequency of expression and increased genetic control and which
considers only environmentally induced traits. Genetic accommodation,
by contrast, applies to both mutationally and environmentally induced
novelties and can either raise or lower the frequency of expression of a
trait by lowering or raising the threshold for its expression or by effects
on the liability to produce a response. Moreover, it includes genetic mod-
ification of trait form, in addition to regulation. It also can result in more
or less genetic control of the phenotype: when environmental sensitivity
is advantageous, genetic accommodation can act to favor it; and if some
environmental factor is essential for the development of the trait, genetic
accommodation would favor such traits as habitat selection and other



906 MARY JANE WEST-EBERHARD

kinds of “niche construction” (Odling-Smee, Laland, and Feldman 2003)
that increase the probability of access to those factors. Genetic accom-
modation, then, can explain how conditional alternative behavioral phe-
notypes and polyphenisms can originate, beginning with an environmen-
tally induced novelty that evolves, under genetic accommodation, to be
maintained as an adaptive alternative to an established trait. Genetic
assimilation, by contrasts, envisions only evolution toward fixation (in-
creased frequency and genetic control).

Genetic accommodation is a universally applicable concept, not an
exceptional one applicable only to special cases in the evolution of novelty.
It describes the genetic response that is expected whenever a polygenic
novel or established trait comes under a new regime of natural selection.
In this sense, it is nothing new: genetic accommodation is simply the
quantitative genetic response to selection on polygenic thresholds and the
coexpressed sets of genes of the “downstream” traits whose expression
the threshold-affecting gene modulates or controls. This is a thoroughly
documented and formally well-characterized process (see, e.g., Falconer
and Mackay 1996). Given the modular nature of discrete phenotypic
novelties, genetic accommodation is the necessary substitute for a single-
locus model of change that implies an erroneous one-gene, one-phenotype
view of the genetic architecture of evolving traits.

4.3. The Nature and Origin of Selectable Variation. In this proposal,
much of the phenotypic change in the origin of novelty is reorganizational,
a product of reexpression of preexisting sets of genes. Reorganizational
phenotypic change, or developmental recombination (West-Eberhard
2003), is based on modular dissociability—it is like moving the furniture.
Modular organization of the phenotype and adaptive phenotypic accom-
modation (West-Eberhard 2003, 2005) permits what Kirschner and Ger-
hart (2005) call “facilitated variation,” variation that capitalizes on al-
ready functional subunits for the assembly of new structures.

One might well ask if there is any real novelty, given the prominence
of reorganizational change, which characterizes even genomic “muta-
tions,” which in turn often involve duplication and reorganization of DNA
subunits (see diverse examples in West-Eberhard 2003, Chapter 17). But
there is one kind of evolutionary change whose true novelty cannot be
denied, and that is the kind that occurs when a lineage incorporates some
new element from the external environment. The heme group of the he-
moglobin molecule is a good example. This is a true novelty. No amount
of reorganization can explain the iron atom in hemoglobin, and genes
cannot make it by themselves. True novelties also arose with the advent
of calcified shells during the Cambrian explosion, when calcium became
newly common in the oceans; with the novel incorporation of essential



MODERN THEORY OF EVOLUTIONARY NOVELTY 907

vitamins or microorganisms that aid digestion in cows, termites, and
aphids; and with the incorporation of luminescent bacteria into the light
organs of some marine invertebrates. No amount of reorganization could
account for the origin of novel form that depends on new elements from
outside the organism for its innovative nature.

5. Conclusion. Whether or not the scheme for the origin of novel traits
that I have outlined above is completely convincing, we are in an exciting
era for biologists and philosophers who aspire to formulate a complete
causal theory of evolutionary novelties. We no longer have to guess at
the mechanisms of inheritance and development. But modern molecular
genomics and evolutionary developmental biology, important sources of
the new information, still pay too little attention to the developmental
role of the environment. I find it remarkable that we have yet to achieve
the comprehensiveness of Darwin’s original theory of novelty, and we will
not match it until there is a wider appreciation of the role of the envi-
ronment in the production of the selectable variation that creates novel
form.

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