Developmental Systems Theory Formulated as a Claim about Inherited Representations*


Developmental Systems Theory Formulated as a Claim about Inherited Representations*
Author(s): Nicholas Shea
Source: Philosophy of Science, Vol. 78, No. 1 (January 2011), pp. 60-82
Published by: The University of Chicago Press on behalf of the Philosophy of Science Association
Stable URL: http://www.jstor.org/stable/10.1086/658110 .
Accessed: 08/07/2013 07:31

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp

 .
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.

 .

The University of Chicago Press and Philosophy of Science Association are collaborating with JSTOR to
digitize, preserve and extend access to Philosophy of Science.

http://www.jstor.org 

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=ucpress
http://www.jstor.org/action/showPublisher?publisherCode=psa
http://www.jstor.org/stable/10.1086/658110?origin=JSTOR-pdf
http://www.jstor.org/page/info/about/policies/terms.jsp
http://www.jstor.org/page/info/about/policies/terms.jsp


Philosophy of Science, 78 (January 2011) pp. 60–82. 0031-8248/2011/7801-0004$10.00
Copyright 2011 by the Philosophy of Science Association. All rights reserved.

60

Developmental Systems Theory
Formulated as a Claim about Inherited

Representations*

Nicholas Shea†‡

Developmental systems theory (DST) is often dismissed on the basis that the causal
indispensability of nongenetic factors in evolution and development has long been
appreciated. A reformulation makes a more substantive claim: that the special role
played by genes is also played by some (but not all) nongenetic resources. That special
role can be captured by Shea’s ‘inherited representation’. Formulating DST as the
claim that there are nongenetic inherited representations turns it into a striking, em-
pirically testable hypothesis. DST’s characteristic rejection of a gene versus environment
dichotomy is preserved but without dissolving into an interactionist casual soup, as
some have alleged.

1. Introduction. Developmental systems theory (DST) has a problem. Not
one of credibility: DST is taken seriously by many philosophers and en-
dorsed by some. Rather, it faces a problem of perceived inutility. Despite
its empirical roots, it motivates relatively little research. That is a loss

*Received October 2009; revised March 2010.

†To contact the author, please write to: Somerville College and Faculty of Philosophy,
University of Oxford, 10 Merton Street, Oxford OX1 4JJ, United Kingdom.

‡For helpful comments and discussion of this material, the author would like to thank
Paul Griffiths, Arnon Levy, Russell Powell, Ulrich Stegmann, Tobias Uller, the referees
for this journal, and audiences in Oxford and at the symposium on Information and
Biological Development at the ISHPSSB meeting in Exeter, July 2007. The research
reported here was supported by the Oxford University Press John Fell Research Fund,
the James Martin 21st Century School, the Wellcome Centre for Neuroethics, and the
Mary Somerville Junior Research Fellowship, Somerville College, University of Ox-
ford.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 61

because DST carries an important message about the evolutionary sig-
nificance of nongenetic factors, the truth of which is only now being
appreciated more widely. Failing to receive credit where it is due would
be merely a pity. Of more consequence is that its perceived lack of utility
is continuing to detract from the ability of DST to make its case.

This article argues that one element of the DST canon, its rejection of
the notion of genetic information, has been an obstacle to the theory
connecting with its target. In arguing that nongenetic factors are critically
important, DST has tended to overshoot and suggest that all causal factors
are on a par. To make the case against gene centrism, DST should be
pointing to the undoubted specialness of genes and saying, “You know
that property, the one that makes genes so special? Well that property is
found not just in genes but in several other factors in development.” That
special role is to transmit information, generated through a process of
natural selection, down the generations to inform development. This ar-
ticle makes use of my treatment of inherited representations to give an
account of that role (Shea 2007).

Relying on a notion of genetic representation will be anathema to many
DST theorists (Moss 2001), especially Susan Oyama, who identifies in-
formation talk as the source of gene centrism and genetic determinism
(Oyama 1985). The claim that genes transmit inherited representations
does not have these consequences, so this is intended as a friendly amend-
ment. The research programme of DST can survive even if we do not
accept the rejection of the existence of genetic information that is central
to DST’s philosophy of nature (following a distinction made by Godfrey-
Smith 2001). The aim is to preserve DST’s key insight about the devel-
opmental and evolutionary importance of nongenetic factors (Griffiths
and Gray 1994). That insight is not yet incorporated into the standard
orthodoxy of the biological sciences, so there is still work for a reinvig-
orated DST to do.

Section 2 argues that DST should go for weaker explanatory parity:
that some but not all developmental factors are on a par with genes.
Section 3 outlines the theory of inherited representations, and section 4
shows how it plausibly applies to a tightly constrained class of nongenetic
factors. Section 5 canvasses some rival proposals for narrowing the parity
thesis. Finally, section 6 argues that inherited representation is better
suited to expressing DST’s central hypothesis than are other accounts of
genetic information.

2. Explanatory Parity in DST. DST encompasses a variety of views. Our
focus is Griffiths and Gray’s parity thesis: that genetic and nongenetic
factors are on a par in development. This section sets out two versions

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


62 NICHOLAS SHEA

of the parity thesis and commends the more limited form according to
which only some other developmental resources are on a par with genes.

Factors other than DNA are clearly causally indispensible in the de-
velopment of an organism. DNA’s initial translation into proteins relies
on there already being machinery in the zygotic cell to perform that task.
Many other non-DNA factors in the cell are also crucial to an organism’s
development: DNA methylation patterns and other chromatin marks,
basal bodies, microtubule organizing centers, cytoplasmic chemical gra-
dients, and so on.

DST goes further, arguing for the evolutionary importance of devel-
opmental factors outside the egg. For example, a supply of vitamin C is
crucial to normal mammalian development. Primates’ diet has contained
vitamin C for so long that they have lost the mammalian ability to syn-
thesize it, making primates reliant on vitamin C in their environment.
Hermit crabs’ development depends on a ready supply of appropriate
empty shells. This too has evolutionary significance. Their use of discarded
shells, rather than growing their own, is doubtless a trait that has evolved
by natural selection. Furthermore, their fitness depends on which shells
are available in the local ecology.

These kinds of examples lead DST to claim explanatory parity between
genes and all nongenetic factors: “The full range of developmental re-
sources represents a complex system that is replicated in development”
(Griffiths and Gray 1994, 275); “Every element of the developmental
matrix which is replicated in each generation and which plays a role in
the production of the evolved life-cycle of the organism is inherited”
(Griffiths and Gray 1997, 474); “[DST has] a wider conception of the
developmental system, not as emerging from interactions between genes,
but as emerging from interactions between the whole matrix of resources
that are required for development” (Griffiths and Gray 2005, 423). In
these passages, DST extends parity very widely. All factors that are caus-
ally involved in species-typical development are put on a par. If that is
right, DST appears to be saying nothing new. It has long been clear that
development is a complex process that depends causally on both genetic
and nongenetic factors. No one doubts that organisms would fail to de-
velop normally in the absence of gravity, say (one of DST’s examples).
DST seems here to be doing no more than emphasizing the causal im-
portance of nongenetic factors in development: each is such that some
aspect of the adaptive phenotype would not develop but for it. Indeed,
Griffiths and Gray sometimes reject the possibility of making a principled
distinction according to which only a subset of other factors is on a par
with genes: “There is much to be said about the different roles of particular
resources. But there is nothing that divides the resources into two fun-
damental kinds” (1994, 277).

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 63

In other places, DST theorists adopt a weaker parity thesis, according
to which there are many distinctions that can be made between factors
found in a developmental system, among which some but not all non-
genetic factors are on a par with genes (Griffiths and Knight 1998, 254;
the ‘more conservative view’ mentioned in Griffiths [2001], 399). But they
do not offer a clear account of what distinguishes the special develop-
mental causes: if not all, which ones are on a par with genes? DST theorists
distance themselves from the claim that ‘genes are not important’, saying
that is a (common) misunderstanding of their position (Griffiths and Gray
2005, 420). Equally, they reject the claim that ‘all developmental causes
are of equal importance’ as being a parody of their position (Griffiths
and Knight 1998, 254). In this more recent work, Griffiths and his coau-
thors make clear that the weaker parity thesis best expresses their view.
However, to avoid being understood in these ways, DST needs an account
of what the importance of genes amounts to, in the DST worldview, and
of why some developmental causes are important in the same way. It
could then substantiate a bold empirical claim: that there are nongenetic
developmental resources that are on a par with genes.

What, though, is the special property of genes that is shared by some,
but not all, nongenetic causes in development? The next section argues
that it is to carry inherited representations.

3. Inherited Representations. This section outlines the argument from
Shea (2007) that genes carry inherited representations. We should clear
away a preliminary objection. Information talk in biology has various
bad associations. The claim that genes are information carriers is taken
by some to imply genetic determinism (cf. Oyama 1985) or that all gene-
environment interactions are additive (cf. Lewontin 1974) or that phe-
notypes come preformed in the genes.

I do not doubt that talk of genetic information can attract these un-
fortunate connotations. As Griffiths has observed (2005), genetic deter-
minism is a popular idea that resolutely refuses to die. However, ‘inherited
representation’ in the theoretical sense developed by Shea (2007) does not
have these implications. Genetic representations can be false, and the
instructions they carry can go unsatisfied. Genetic representations do not
contain preformed phenotypic outcomes, and they do not determine such
outcomes. Nor does the existence of genetic representation presuppose
that gene-environment interactions are additive. So these motivations for
resisting information talk furnish no good reason to reject the existence
of inherited representations in the sense offered here.

Griffiths and Gray have a second objection to accounts of genetic
information, which is that they fail in the stated aim of capturing a special
role played by genes. There is correlational information whenever, for some

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


64 NICHOLAS SHEA

univocal reason, the state of one system changes the probability that some
other system instantiates some property. Shannon’s treatment emphasizes
that the way that the states of two systems correlate depends on which
background ‘channel conditions’ are held fixed (Shannon 1949; Dretske
1981). Genes carry information about genotypes in this sense, if we treat
the circumstances of development as channel conditions that are held
fixed. However, Griffiths and Gray (1994) are right to observe that we
can equally well fix on the genome as a channel condition, against which
variations in the developmental environment will also carry Shannon in-
formation about phenotypes.

In response, various theorists argued that genes carry information in
a stronger sense than mere correlations—that they carry semantic infor-
mation, with correctness conditions or satisfaction conditions (i.e., that
they are representations). Sterelny, Smith, and Dickison (1996) and May-
nard Smith (2000) founded that claim on evolutionary functions—on the
function of genes to produce the outcomes for which they have been
selected.1 These proposals still appeared too liberal, attributing semantic
information to not only genes but every factor in development that has
an evolutionary function. To counter those objections, Shea (2007) argued
that a careful application of the framework of teleosemantics to the ge-
nome requires more than just evolutionary functions. I differed from ear-
lier authors in taking seriously the need to identify a consumer of the
representations carried by the genome (see also Godfrey-Smith 2006).

The teleosemantic framework applies when there is a consumer system
that responds to a range of different representations by producing a range
of different outputs (Millikan 1984). Teleosemantics naturalizes the in-
tuitive idea that a token is a representation when a system treats it as a
proxy for some further fact C about the world. The system responds to
the token in a way that is appropriate, given that C obtains. A gene or
genotype G is selected because a phenotypic feature P with which it cor-
relates is conducive to some feature C of the environment (including
existing features of the organism). Gene G is then transmitted down the
generations so that descendant organisms continue to develop phenotype
P. Doing so will be adaptive while condition C continues to obtain. If it
were right to characterize the production of P by the mechanisms of
development, on the basis of reacting to G in the zygote, as the operation
of a consumer system that takes G as input, then it would follow from
teleosemantics that G represents that C obtains.

Is there, then, a consumer for the selected genes that are transmitted
to the zygotes of future generations? Is there a system that has the function

1. Jablonka (2002) also made an ingenious appeal to teleofunctions but in the service
of indicative rather than imperative contents.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 65

of responding to a range of different genotypes by producing a range of
different outputs? Shea (2007) argues that such a consumer can only be
discerned from the perspective of evolutionary time. A single individual
has access to just one set of zygotic DNA, but over phylogenetic time
within a lineage, development in different individuals encounters a range
of different genotypes and produces a range of different adaptive phe-
notypes in response. Viewed over phylogenetic time, development seems
to be acting as a consumer. But is that its function? Does development
have the evolutionary function of responding to a range of different ge-
notypes with a range of different phenotypes?

That is a very demanding constraint. Godfrey-Smith (1999) argues that,
in addition to functions of particular genes (his option A), DNA in general
may have adaptive functions (option B). Particular genes that are the
basis of heritable phenotypes, and have been selected, have teleofunctions
under option A. But there is also evidence that the DNA system as a
whole, with its mechanisms of transcription, translation, and replication,
and of proofreading and repair, also has a teleofunction under option B:
the function of transmitting phenotypes down the generations. That func-
tion is a higher-order or metalevel function, in that it is not the function
to produce any particular object-level trait X but to produce whatever
traits have been selected. Developmental resources that have this meta-
function are inheritance systems. If the genome and the associated ma-
chinery of development is an inheritance system, then development does
indeed have the metafunction of responding to a range of different ge-
notypes with a range of different phenotypes. So it would qualify as a
genuine consumer system.

It is a substantial, but plausible, empirical commitment of the theory
that DNA does have this metafunction. Bergstrom and Rosvall (forth-
coming) point out that DNA is extraordinarily good at storing and trans-
mitting an arbitrary sequence since it is inert, structurally stable, and very
easy to replicate, and can store a long and indefinitely extensible sequence
in a small space. These features do not yet show that DNA has our exotic
metafunction because they may just be the cause of the powerful evolution
we have on earth, without being the consequence of some earlier evolu-
tionary process. Maynard Smith and Szathmáry (1995) go further, arguing
that DNA-based inheritance evolved out of an RNA world because of
the increased fidelity with which DNA transmits selected phenotypes down
the generations. Furthermore, there are two stronger lines of evidence
that do not depend on the origins of DNA being based on selection for
the metafunction.

It is likely that the DNA transmission system has been modified in
various ways in order to perform the metafunction of transmitting selected
phenotypes. First, the mechanisms of DNA proofreading and repair are,

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


66 NICHOLAS SHEA

very plausibly, adaptations for improved transmission fidelity (Alberts et
al. 2004, 169–91). They cannot be explained away as adaptations for
somatic cell inheritance since they are also found in single-celled organ-
isms. The second line of evidence turns on the degrees of freedom in the
code that links nucleotide triplets to amino acids. The pairings we observe
today are not based on any chemical specificity between nucleotides and
amino acids but just depend on how the mechanisms of translation are
set up. It seems that there has been selection on the triplet–amino acid
mapping, sometime in the distant evolutionary past (Haig and Hurst 1991;
Freeland and Hurst 1998). Out of all the millions of possible triplet–
amino acid codes, it seems that the code we have is optimized to reduce
the impact of common replication errors (as well as translation errors).
The most common errors produce amino acids with similar chemical prop-
erties, hence, proteins with similar enzymatic activity. Both of these mod-
ifications of the DNA-development system suggest that it has evolved to
perform the metafunction of transmitting selected phenotypes, irrespective
of why it originally came into existence.2 An analogy is the way we stick
a piece of felt onto a rock to make it function as a good paperweight.

Given the metafunction, teleosemantics shows how zygotic DNA carries
representational content. A gene G is selected for a heritable phenotypic
difference P that it makes (in a certain population, across the range of
environments in which it is found).3 Once selected, G will then be trans-
mitted to the zygotic DNA of generations of future organisms, which will
continue to develop phenotype P. Gene G may subsequently come to be
causally involved in very many phenotypic effects, in combination with
other genes or features of the environment, but according to the standard
modern synthesis there is a fact of the matter about the phenotypic effect
P for which it was originally selected. There is also a fact about the
conditions of the selective environment that were conducive to P (why
there was selection for P). Only when that condition C obtains does P
continue to perform its function in an evolutionarily normal way (i.e., in
the way that accounts for its having been selected). The obtaining of C
is a success condition for the output P that the consumer system produces
in response to G. It follows that G has the indicative content C is the

2. There is a legitimate question about how such selection could have happened. Lin-
eage-based selection is a candidate, especially since DNA’s metafunction is likely to
be evolutionarily ancient, coming before the evolution of multicellularity. An alternative
is that the benefits in long-run fitness achieved through improvements in transmission
fidelity can be an effective way for machinery with such a metafunction to evolve, if
the short-run fitness costs of increased fidelity are zero or very small.

3. The same story applies to asexual organisms but at the level of the whole genome,
in virtue of selection between different genomes.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 67

case. And the consumer must continue to produce P in response to G if
it is to perform its function in an evolutionarily normal way. So teleo-
semantics also ascribes to G the imperative content develop P. The in-
dicative content will be false if the environment changes so that C no
longer obtains, and the imperative content will go unsatisfied if, because
of error or subsequent selection, development fails to produce P in re-
sponse to G.

One of the starting points for the account of genetic representation in
Shea (2007) was Moss’s (2001) influential distinction between the gene D
(the causal role of a molecular gene in development) and the gene P
(genetic differences that correlate with phenotypic differences). Moss
makes a detailed critique of the gene-as-information based on the relative
rarity of genes P for interesting phenotypes (genetic diseases aside) and
offers DST the noninformational gene D instead. Shea (2007) argues that
genetic representation is based not on current genes P but on the existence
of a gene P at the time when a phenotype was selected, as required for
evolution by natural selection. That opens up a substantial notion of gene-
as-information that DST can make use of.

In some cases, G may have been selected because it produced a range
of phenotypic effects (P1, . . . , Pn), each being conducive to different
features of the selective environment (C1, . . . , Cn). In that case, we need
a more complex sentence to capture the content of G: C1 and . . . and
Cn is the case; develop P1 or . . . or Pn. In cases of adaptive plasticity,
the different phenotypic effects may be adapted to variable features of
environment (V1, . . . , Vn), with development being cued to variations
in the environment in some way. If G is selected for these reasons, it will
come to carry the content: V1 or . . . or Vn is the case; develop P1 if V1,
. . . , Pn if Vn.

Notice that, even if a gene is selected for a range of phenotypic effects,
this is a small subset of the phenotypes in which it is involved causally.
Pleiotropy and polygeny are ubiquitous, so most genes will be involved
in the production of very many different phenotypes, and most phenotypes
depend on the expression of very many different genes. Nevertheless, the
evolutionary story about why a given gene was selected involves only a
small subset of these effects. In any particular case, it may be very hard
to tell why a given gene was selected, but if evolutionary orthodoxy is
even roughly true, then there has been cumulative selection with genes
each being selected for some relatively small number of phenotypes.

Relatedly, observe that the sense in which genes represent phenotypes
does not imply a tight causal connection between genes and phenotypes.
Natural selection just requires a gene-phenotype correlation to be heri-
table. That connection may be completely contingent, being highly de-
pendent on particular features of the environment in which it was selected

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


68 NICHOLAS SHEA

(that happened to be stable enough at the time of selection). It may also
depend heavily on the genetic background against which that variation
occurred. So when a genotype G represents a particular phenotype P, it
in no way follows that G specifies P or causally determines P in any
environments outside the range in which it was selected. Even the language
of G ‘programming for’ P suggests some kind of tight causal connection
between genotype and phenotype. The notion of inherited representation
does not have those consequences.

One of the motivations for DST was Lewontin’s criticism of the ‘lock
and key’ model of evolution (Griffiths and Gray 2005, 418). Lewontin
(1982, 1983) argued that thinking of organisms as being adapted to pre-
existing niches or available ways of life underestimates the extent to which
organisms construct their own niches. Our approach to genetic represen-
tation can capture such cases, where the indicative content is some very
general fact about the environment, but the imperative content is a rich
specification of a particular phenotype. That is a further strand of DST
that can be nicely expressed using the concept of inherited representation.

This article aims to show that a teleosemantic account of inherited
representation is adequate to the task of expressing the fundamental in-
sight of DST. I do not argue that no other account of genetic represen-
tation could do so. I deal with the main rivals in the literature, but it
remains open that a different account of genetic representation, grounded,
for example, in control theory, may turn out to be adequate to the same
task. If I am wrong about DNA’s metafunction, then another account of
inherited representation would needed if it is to be used to precisify the
claims of DST (the unavailability of which might then motivate a strong
version of the parity thesis).

4. Inherited Representations in Other Inheritance Systems. My account of
inherited representation is defended in detail in Shea (2007), but the outline
above is enough to see how it applies to some, but by no means all, other
causal factors in development. The crucial issue is whether a develop-
mental resource is part of an inheritance system, that is, whether it has
the metafunction of transmitting selected phenotypes down the genera-
tions. Only then will it carry inherited representations.

An example illustrates that many functionally important causal factors
are excluded. In Drosophila melanogaster, the way the embryo differen-
tiates into different cell types, so as to form the insect’s gross morphology,
is driven by concentration gradients of various proteins in the embryo.
Initially, these come from maternally derived morphogens (mRNA and
the proteins themselves) placed directly into the cytoplasm of the zygote.
So initial morphological development is not under the causal influence of
the zygote’s own DNA. Maternally derived morphogens are part of the

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 69

zygote’s inheritance in a wide sense but are not heritable. When experi-
mentally induced variations lead to viable phenotypic differences (with
the genetic background held fixed), descent stops at the first generation.
The morphogens that the first offspring passes to the zygotes it produces
depend on DNA expression and are independent of the configuration of
morphogens it received from its mother. By contrast, genetic variation
does lead to heritable differences in the way morphogens are passed down
the generations (and in resulting morphology). These genetic variants are
maternal effect mutants: the effect of the genetic variation is first seen in
offspring and is then carried down the generations (Weber 2005, chap.
8).

Maternally derived morphogens are causally indispensable to the or-
ganism’s development. They count as ‘inherited’ on the wide understand-
ing adopted by DST.4 But they are of only very limited significance to
evolutionary questions since changes in morphogen gradients are not
transmitted far into the future unless those changes are based on genetic
changes. They are part of the causal background to the organism’s de-
velopment, along with myriad other crucial causal factors, but their lim-
ited evolutionary significance is reflected in the fact that they do not carry
inherited representations.

However, inherited representations are likely to be carried by factors
other than the genome. Recent years have seen an explosion of research
on transgenerational epigenetic inheritance: mechanisms by which the
state of activity of genes is passed on to future generations. For example,
gene expression is modulated by modifications to the DNA envelope,
including through methylating stretches of chromatin. The wealth of evi-
dence summarized in Jablonka and Raz (2009) shows that epigenetic
effects are found in almost every form of life and that many are very long
lasting. Given their ubiquity, it is very likely that, as with DNA, there
has been selection on epigenetic mechanisms like chromatin marking for
the way they transmit selected phenotypes down the generations. So it is
very plausible that some epigenetic mechanisms form an inheritance sys-
tem and so carry inherited representations.

Compare cell membrane structures. When the zygote divides to form
a multicelled embryo, it needs to synthesize new cell walls. That process
crucially depends on the structure of the zygote’s own cell wall and as-
sociated elements like centrioles and microtubule organizing centers
(which were constructed for the zygote by its mother and which it ‘inherits’
in DST’s broad sense). Unlike the morphogen gradients in Drosophila,
some changes to cell wall structures may be heritable, giving rise to long-

4. Griffiths (2001) treats as inheritance “any biological mechanism that produces re-
semblances between parents and offspring” (399–400).

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


70 NICHOLAS SHEA

term differences in generations of descendants. (Such differences can thus
be subject to natural selection.) However, it is much less plausible that
cell walls have the relevant metafunction. It is unlikely that there has been
selection on this system for the way it transmits phenotypes in general
down the generations, especially as the range of variation of outcomes is
limited. So it is unlikely that cell wall structures are inheritance systems,
falling into the class of interesting cases that make DST a thesis with
strong empirical bite.

A final example is learning by imitation. Here, plausibly, evolution has
invented a new channel or channels of inheritance, but the test is de-
manding. Very many kinds of socially mediated learning give rise to be-
havioral traditions, even through low-level social phenomena like local
enhancement (Avital and Jablonka 2000). Once there are transmitted her-
itable differences, natural selection may act to select the fitter variant
(Mameli 2004), but there are few examples in other animals of cumulative
selection of behavioral phenotypes that build on one another,5 without
the operation of gene-based selection. That is much more likely to occur
if the learning mechanism has been adapted to the function of transmitting
selected (behavioral) phenotypes down the generations.

There is some evidence that there is a form of imitative learning, at
least in humans, that has been adapted to perform this function (Shea
2009). Humans exhibit ‘blind overimitation’, copying the details of the
way an observed action is performed, even though they can see a more
efficient route to the same result. By contrast, chimps go directly for the
demonstrated outcome, cutting out unnecessary actions and employing
the most efficient means of achieving the reward. There is even evidence
for a developmental trajectory in humans, with younger children per-
forming more like chimps and the disposition for blind overimitation
emerging only between 3 and 5 years of age (Whiten et al. 2009). At first
glance, the chimps have the more rational strategy. If you can see an easier
way of reaching the result, why copy additional details of the demon-
strator’s action sequence? On reflection, though, we can see that the hu-
man strategy could be an adaptation for transmission fidelity. It allows
behavioral phenotypes to be transmitted down the generations, even if
their utility cannot be checked by any individual—which would be useful
if the advantages of the behavioral variant are too long term or stochastic
to be reliably detectable by an individual (e.g., the long-term benefits of
particular food preparation practices). By contrast, chimps appear to be
learning for themselves, using observed behavior as a helpful cue. The
otherwise-puzzling disposition for blind overimitation together with some

5. See the examples in Avital and Jablonka (2000).

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 71

other features of human imitative learning suggest that it may have been
modified in order to perform the function of transmitting selected be-
havioral phenotypes (Shea 2009). In that case, it is a further inheritance
system: an additional channel by which information, generated by a pro-
cess of selection over many generations, is transmitted to future gener-
ations to allow them to produce adaptive phenotypes.

This summary of other putative inheritance systems suggests that the
parity thesis is correct, on the weaker reading (Griffiths 2001, 396): a
defensible notion of genetic information does also apply to other causal
factors in development, like chromatin marking. That was a prescient
insight of DST. The theory’s only mistake was, at times, to take such
examples to motivate an overly inclusive parity thesis. There is no good
reason to treat environmental resources like the shells used by hermit
crabs, or primates’ dietary vitamin C, as carrying information down the
generations in any substantive sense. Inherited representation sharply de-
lineates a subclass of resources that have an important explanatory status.

With the recent upwelling of research discovering extragenetic mech-
anisms of inheritance all over the place, it is easy to forget just how
unorthodox the DST message originally was. DST traces its roots back
to Lehrman in the 1950s and the developmental psychobiology of Gottlieb
in the 1960s (Griffiths and Gray 2005, 418), when extragenetic inheritance
was decidedly a minority interest. Gene centrism became, if anything,
only more dominant with the success of models of gene-based selection
in the 1970s (e.g., of altruism) and the rise of molecular biology in the
1980s. DST theorists faced a formidable task to persuade the biological
community that extragenetic inheritance was more than a rare curiosity.
In the 10 years between Jablonka and Lamb’s books (1995, 2005), the
tide began to turn in favor of the prevalence and importance of mecha-
nisms of extragenetic inheritance. That prescient insight should be DST’s
key message. It is succinctly captured by the claim that, in addition to
the genome, there are other developmental factors that carry inherited
representations.

5. Rival Candidates for Narrowing the Parity Thesis.

5.1. Three Nested Classes. So far, we have seen that inherited repre-
sentation is eminently suited to formulating DST’s thesis about the de-
velopmental and evolutionary importance of nongenetic factors. In this
section, we argue that inherited representation is the best candidate for
formulating DST as a radical empirical hypothesis.

DST is interested in developmental causes that recur in each cycle of
development, so it excludes one-off accidents (Griffiths and Gray 1994,

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


72 NICHOLAS SHEA

286). Among such recurring causal factors, we consider three progressive
narrowings that form a nested set of subclasses: C1, C2, and C3.

Some recurring factors are not functional, for example, traits that have
evolved by genetic drift. DST could formulate its parity thesis as: genes
are on a par with all other developmental factors that have evolutionary
functions (class C1). Evolutionary functions are effects that enter into an
explanation of the survival and reproduction of the entities that produce
those effects. One of Griffiths and Gray’s examples (1994) is the way
ducklings’ preference for the maternal call of their own species depends
on hearing their own, different, call while they are still in the egg. It
follows that one of the functions of ducklings’ prenatal vocalizations is,
surprisingly, to produce a preference for the maternal call. Many of DST’s
favorite examples fall into this category. A mother rat’s disposition to lick
the genitalia of her male pups has the function of promoting the nerve
supply needed for normal penile function. DST also wants to treat as
functional the interactions between an organism and the background con-
ditions of its environment: a plant’s location on the earth’s surface where
there is sun, an animal’s interaction with gravity while it grows, primates’
interaction with vitamin C in their fruit diet, and hermit crabs’ interaction
with other species’ shells. Griffiths and Gray (1994, 290–92) emphasize
that such processes should be given an evolutionary explanation, so they,
too, plausibly fall into class C1.

Pointing out that factors other than genes have evolutionary functions
is no kind of revelation. In many places, DST theorists focus on a more
interesting fact: that there are developmental factors other than genes that
give rise to heritable phenotypes. A genetic change in the germ line, if
viable, causes a phenotypic difference in a long lineage of descendants.
Recall the morphogen gradients in Drosophila. Changing a morphogen
gradient in the zygote can make a viable phenotypic difference in that
individual but goes no further. Changing a gene whose expression is re-
sponsible for that morphogen causes a phenotypic effect that is trans-
mitted down the generations. When variation in a developmental factor
causes phenotypic variation that is heritable, natural selection can act so
that the population evolves toward the fitter variant. Evolution crucially
depends on the fact that genetic variation produces heritable phenotypic
variation.

In more concessive moments, when DST theorists hint that they do
not really think that all developmental resources are on a par, they suggest
that this is the class of interest. Gray uses heritability as the acid test of
whether developmental resources are transmitted extragenetically (2001,
sec. 9.7, 194–96). Griffiths lists various factors that are on a par with
genes ‘on the more conservative view’ and characterizes them as follows:
“Changes in these other resources can cause heritable variation that ap-

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 73

pears in all the cells descended from that egg cell” (2001, 400). That is
our second candidate narrowing, C2: causes of heritable phenotypic var-
iation.6

The examples of class C1 discussed above were chosen so as to fall
outside class C2. Class C2 also excludes some other cases from the DST
literature, for example, some varieties of niche construction. A new termite
colony gets a head start in life if it can inhabit an existing termite mound,
but changes made directly to the mound are not preserved and transmitted
down the generations to further colonies in further mounds (as they would
be if caused by a genetic difference). Similarly, changes made directly to
beaver dams are unlikely to be heritable. Nevertheless, C2 does capture
many of DST’s most central examples. Male cowbirds have different song
dialects in different regions, without any relevant genetic differences. The
male learns the regionally appropriate song partly through feedback from
females with a preference for the local song. Given this mechanism,
changes to the phenotype (the local song dialect) will end up being trans-
mitted down the generations.

It is unclear that there has been selection between the different songs
sung in different subpopulations, but where heritable differences do have
fitness consequences, selection can act, even if there are no relevant genetic
differences (Mameli 2004). Habitat imprinting is the process by which
animals prefer to live in the type of habitat in which they grew up. Ap-
parently, when one population of European mistle thrushes imprinted on
parkland, it did better than populations imprinted on forest (cited by
Immelmann 1975). The parkland population expanded not because of a
genetic difference, or because of continuing transfers from forest popu-
lations, but because of the increased fitness of those individuals that had
acquired the parkland habit from their forebears. Class C2 also covers
socially transmitted food preferences in rats. A disposition to eat what
your mother eats will give rise to behavioral traditions, and, depending
on the extent of individual learning, selection could act on those differ-
ences. Griffiths and Gray argue that cuckoolike brood parasitism in vi-
duine finches shows selection on imprinting-based variants (1994, 289–
90). Offspring lay their eggs in the nest of the species that brought them
up, and there are different subspecies imprinted on parasitizing different
host species (although in this case there are genetically based morpho-
logical differences as well).

These examples fall into the very broad class of Darwinian processes

6. Once a heritable phenotype has been genetically selected, it may cease to be heritable,
both because of subsequent pleiotropy and epistasis or because of changes in the
makeup of the population or developmental environment. The selected gene will con-
tinue to be a cause of the transmission of the selected phenotype down the generations.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


74 NICHOLAS SHEA

(Godfrey-Smith 2007), and they are clearly of importance in characterizing
the evolutionary dynamics. As with any kind of learning, they change the
space of possibilities that lie on accessible evolutionary trajectories. But
imprinting is an extremely limited mechanism for passing on adaptive
phenotypes. When a population becomes imprinted on a new habitat or
resource, the previous phenotype is replaced. No accumulation of ad-
aptations is possible. Most of the pattern can be understood as a con-
sequence of a genetically based adaptation for habitat imprinting. DST’s
fire ant example is similar. Whether a queen is large and monogynous or
small and polygynous depends on a pheromone that is produced by and
persists in the respective colonies. Thus, the phenotypic difference is her-
itable because of an environmental factor, the pheromone, that is trans-
mitted down the generations. But again, this is a very limited system of
heredity. Although the pheromonal differences may be used to trigger a
variety of changes, there is only a very limited range of variation in the
transmitted resource (the pheromone).

In their most concessive moments, some DST theorists seem to be
pointing to something much more radical. Gray argues that DST research
should “investigate whether there are adaptive mechanisms for passing on
extragenetic inheritance” (2001, 202; emphasis added). If there are other
mechanisms for passing on selected phenotypes, in addition to genes, then
they would show more than the limited selection between exclusive al-
ternatives illustrated by imprinting. They would enable the accumulation
of adaptations. This is the most restrictive narrowing, class C3: the class
of interest for DST should be mechanisms with the evolutionary function
of transmitting selected phenotypes down the generations. Sterelny (2001)
argues for a related distinction based on evolvability—as we will see in
the next subsection.

5.2. Class C3 versus Inherited Representation. Class C3 is the class of
factors that have the metafunction we relied on earlier as underpinning
the existence of inherited representations (sec. 3). We saw in section 4 that
there are plausible examples of nongenetic factors with this metafunction
(chromatin marking, blind overimitation in humans). If the importance
of class C3 is accepted, we are most of the way home. The only remaining
question is, what is the benefit of using informational properties to draw
the relevant distinction (as we do in sec. 3)—of formulating DST’s hy-
pothesis in terms of inherited representations?

We offer three reasons for understanding inheritance systems (class C3)
as information channels. The first is that evolution does not just depend
on selection and the generation of etiological functions but also requires
information generated by selection to be preserved and transmitted over
very many generations. The process of differential survival and repro-

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 75

duction—selection—generates information about which phenotypic var-
iants are better suited to the environments in which they exist. Life can
only evolve if that information is somehow transmitted to subsequent
generations. DST’s message about the evolutionary importance of non-
genetic factors is at its strongest when we see that factors in class C3 can
solve this informational problem: DNA is a wonderful solution, but there
are others too. The C3 factors are rightly considered to be new information
channels in their own right, precisely because the metafunction that is
definitive of class C3 underpins inherited representation.

At one point, Griffiths and Gray appear to accept an informational
take on heredity, as one of many distinctions that can be drawn legiti-
mately between different causal factors involved in development. Al-
though sticking to DST’s overall claim that no dichotomy between dif-
ferent factors in development should be privileged, Griffiths and Gray
accept that a distinction between sample-based and information-based
heredity may be useful for some purposes (2005, 420).

Second, it is becoming increasingly clear how right DST theorists were
about the number of different means by which parents have long-lasting
influences on their offspring (Jablonka and Lamb 1995, 2005; and the
very many examples in Jablonka and Raz [2009]). Information is useful
as a common denominator by which all these different systems of heredity
can be compared (Jablonka and Lamb 2007, 382).

The third point relies on the more controversial claim that inherited
representations are read in the course of individual development (Shea,
“Inherited Representations Are Read in Development,” forthcoming).
Understanding class C3 in informational terms allows us to see that in-
heritance channels are one of several different sources of information that
inform individual development, alongside detecting adaptively relevant
information in the individual’s own environment (adaptive phenotypic
plasticity) and receiving informational cues from the previous generation
(cross-generational phenotypic plasticity). Space permits only an outline
of that claim here. The idea is most simply explained using a gene-based
example, but exactly the same point carries over to DST’s examples of
other inheritance systems that have been adapted for transmitting selected
phenotypes.

The idea stretches back to the later Lorenz (1965), in which he argued
that organisms inherit genetic information about the type of environment
they are likely to face and use it to achieve an adaptive match to their
environment. The explanandum is the striking fact that developing or-
ganisms manage to arrive at phenotypes that match aspects of their en-
vironment in functional ways. For example, African horseflies of the genus
Tabanidae pupate in muddy pools (Lambourn 1930). The larva constructs
a cylinder consisting of two corkscrew spirals drilled in opposite directions

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


76 NICHOLAS SHEA

through the mud before forming its pupa in the middle of the cylinder,
bottom center. When the pool evaporates, and the mud dries out and
cracks, the cracks pass neatly around the pupa. The spiral burrowing is
thought to be an adaptation to avoid the risk of the pupation chamber
being split in two by a crack in the surrounding mud. But how does the
larva “know”? That is to say, where does the information come from that
tells the larva that the pupation chamber it is about to construct is at risk
from cracking as the mud dries out? There is a striking match between
the larval phenotype (the spiral burrowing behavior) and a property of
its future environment (cracking mud). DST counsels that we should view
the organism’s relation to its environment as just another aspect of the
unfolding complex developmental system. That perspective overlooks a
pressing explanandum, not about how the relation evolved, to which DST
can offer the standard Darwinian answer, but about where the information
comes from, in individual development, that allows the organism to de-
velop in a way that so exquisitely matches its environment. That explan-
andum cries out for an informational explanation.

In some cases, the organism detects the relevant property directly while
it is developing (Leimar, Hammerstein, and Van Dooren [2006] model the
choice between this and relying on what we have been calling inherited
representations). For example, the water flea Daphnia pulex relies on
chemical traces of predators in the water to tell it whether to grow an
expensive defensive shell. In Tabanidae, natural selection is the more likely
culprit. The standard story about selection on randomly produced genetic
variants means that the genotype that gives rise to the corkscrew bur-
rowing comes to correlate with a fitness-relevant feature of its phylogenetic
environment, namely, that the pupation environment dries out and cracks.
That is information in the correlational sense. The role of information in
the proximal causal story about fly development is thereby connected with
the distal story about the origin of that information in phylogenetic his-
tory. So natural selection not only explains the adaptation, in the usual
way, it also explains how the developing organism manages to solve an
informational problem. The organism narrows its uncertainty about the
nature of the environment in which it will develop by relying on a re-
source—its genotype—that represents a feature of the environment.

Where natural selection generates information in other inheritance sys-
tems (sec. 4), that too informs individual development. For example, if
there has been natural selection on variations in transmitted chromatin
marks, then the selected chromatin mark will carry useful information
about the selective environment, which will guide the organism toward
developing an environmentally appropriate phenotype. Blind overimita-
tion is another example, although there it is easy to overlook the role of
selection in generating the information. At first glance, the imitator seems

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 77

just to be learning from the model. But recall that the imitator may have
no idea why the behavioral phenotype is adaptive (e.g., why a particular
food preparation practice is beneficial, on average in the long run). There
may be no way for an individual to detect the adaptive significance of
the behavior, if the feedback is too stochastic or too long term for an
individual to keep track of. In such cases, the way the behavior of the
model guides the imitator to an adaptive outcome depends on transmis-
sion of information that was generated by selection over very many gen-
erations in the evolutionary past.

Cross-generational phenotypic plasticity (Sultan 2000) is closer to the
within-generation process by which the water flea detects an environ-
mental correlate of predators than to the transgenerational process by
which information generated through natural selection is transmitted to
future generations. Many parental effects arise because the parent can
give its offspring relevant information about its local environment. In
plants, parental effects can convey to the developing seedling useful in-
formation about the kind of local microclimate is it likely to find itself
in and, so, about which morphological variant or life history strategy it
ought to adopt (Galloway and Etterson 2007). The stress-related phe-
notype expressed in mother rats, that causes the offspring in turn to be
highly stress reactive (Meaney 2001), is also plausibly a mechanism
whereby the mother can pass to her offspring (in a rather unobvious way)
adaptively relevant information about the kind of environment they are
likely to find themselves in. These are not mechanisms that have been
adapted for transmitting selected phenotypes (inheritance systems/class
C3). Instead, they are cross-generational signaling mechanisms by which
parents signal an adaptively relevant environmental variable and offspring
produce an adaptively plastic phenotype in response (Shea, “Two Modes
of Transgenerational Information Transmission,” forthcoming). They do
not carry inherited representations but are examples of a different means
by which the developing organism can narrow its uncertainty about its
developmental environment.

In summary, the special role of DNA comes out when we ask an in-
formational question. DST’s insight is that other developmental factors
may play that role too.

6. Other Accounts of Genetic Information. Other accounts of inherited
information have been offered. Shea (2007) has arguments that some of
these fail on their own terms, which we will not reopen here. Others are
perfectly cogent but do not capture the sense in which inheritance systems
transmit representations or semantic information. In this section, we argue
that those accounts are less well suited than inherited representation to
capturing the important claim at the heart of DST.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


78 NICHOLAS SHEA

Levy (2010) argues that information talk is a useful metaphor, allowing
scientists to break down systems into senders and receivers so as to be
able to think about them more easily. In Levy’s view, the usefulness of
such metaphors does not turn on genes really carrying representational
content. The metaphor can be applied in very many situations. So it would
not help DST in singling out a special class of developmental factors
about which to make its claim.

By contrast, Godfrey-Smith (1999, 2000) focuses on a very particular
property of DNA. He argues that it is appropriate to talk about DNA
in informational terms only because of the triplet code, a precise relation
of causal specificity between the linear order of triplet codons on the
DNA molecule and the linear order of amino acids in the proteins that
are expressed. Stegmann (2005) argues that the way that DNA determines
protein products, through template-directed synthesis, makes it an in-
struction to form those products.7 Godfrey-Smith and Stegmann both
appeal to very specific features of the way DNA actually operates, with
little prospect of the same properties being exemplified by any nongenetic
factors. Neither account is suited to the role of locating information in
nongenetic resources (rather, they found an argument to the falsity of
even the weak parity thesis).

Kim Sterelny has been involved in the development of a series of views
about the status of genetic information. Sterelny and Kitcher (1988) ar-
gued that a molecular gene codes for a trait relative to a standard back-
ground of environment and other genes. The problem was to identify the
standard in a principled way. Sterelny et al. (1996) relied on teleology, as
did Maynard Smith (2000), with genes representing the outcomes that it
was their etiological function to produce. As we have seen, very many
developmental factors have evolutionary functions, so these accounts ov-
ergenerate. Jablonka (2002) relied on evolutionary functions to underpin
indicative contents for genes, based on ‘interpreting receivers’. While it
is not entirely clear what physical system corresponds to the receivers,
Jablonka does not have the constraint of the metafunction identified by
Shea (2007), so her account may also overgenerate. Nor does it capture
a sense in which genes have imperative contents.

Sterelny (2001) took a different tack, focusing not on representation
but on what it is to be a replicator, which he identified as the set of

7. Stegmann’s ‘instructional content’ turns on the claim that DNA determines the kind
and order of the operations that will be carried out to produce its protein product.
However, this determination only occurs when conditions are right and things go well.
So Stegmann may need to appeal to teleology (although not teleosemantics) to specify
the circumstances in which effects flowing from DNA count as being among the ‘de-
terminings’ that are relied on in discerning instructional content.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 79

developmental resources that are like DNA in being highly evolvable. A
subsidiary point was that such evolvable systems are unlikely to have
arisen by chance but have probably been adapted for the transmission of
similarity across the generations—that is, to be in our class of inheritance
systems, C3. Sterelny (2001) did much to spell out the conditions that
underpin evolvability. Since carrying inherited representations in our sense
is based on a mechanism having the metafunction that is evidenced by
Sterelny’s evolvability criteria, the two accounts will agree about most of
the cases—about which factors DST should identify as being on a par
with genes from an evolutionary and developmental point of view. My
account differs from Sterelny in two respects, one local and one global.

The local difference is that Sterelny does not think that all inheritance
systems involve information transfer (2001, 346 and 347). Those which
involve transfer of samples from parents to offspring are not cases of
information transmission, in his view. Sterelny (2004) develops the dis-
tinction, spelling out the distinctive evolutionary characteristics of sample-
based inheritance.

In my view, the fact that samples are transferred in a process of in-
heritance does not exclude the fact that information is also transmitted—
that the samples carry representational content (of our ‘inherited repre-
sentation’ variety). There is no such exclusion with representation in gen-
eral. When I ask a baker, “what’s good?” he may just pass me a slice of
cake. The cake is a sample but is also an answer to the question, carrying
a semantic content along the lines of this is good. Similarly, some of the
examples of sample-based inheritance discussed by Sterelny (2001, 2004)
are also cases in which information, generated by a process of selection,
is being transmitted to future generations. If they are adapted for the
transmission of similarity across generations, as Sterelny suggests (2001,
338 and 346), these mechanisms are thereby carrying inherited represen-
tations, for the reasons given in sections 3 and 4 above.

Not all the samples that lead to cross-generational similarity will carry
inherited representations since some may be a cause of cross-generational
similarity (class C2) without being an adaptation for transmitting cross-
generational similarity (C3, which is a proper subset of C2). In an obligate
symbiosis, say between an insect species and a particular digestive bac-
terium, the mechanism for passing on a sample of the bacterium in the
insect’s eggs does not look to have been designed to carry a range of
different messages. Even where there is a range of possible symbionts, as
when juvenile ruminants ingest faeces to acquire microorganisms that are
needed for digestion, the case is more like that of imprinting. The mech-
anism can give rise to heritable features, but that is not its purpose. Its
evolutionary function is to pass on symbiotic microorganisms. Further-
more, some passing of samples may be cases of cross-generational phe-

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


80 NICHOLAS SHEA

notypic plasticity (Sultan 2000, discussed above). In any event, there does
not seem to be anything like the fancy metafunction exemplified by DNA.
So, while some cases of sample-based heredity do not count as trans-
mitting semantic information, some do. Transfer of samples does not
exclude transfer of semantic information.

So much for the local disagreement with the later Sterelny (2001, 2004).
The more global disagreement concerns the importance of information.
Sterelny identifies the class of systems that should be of interest to DST
directly in terms of conditions on evolvability. While this is evidence of
class C3, it is not equivalent. Furthermore, there are explanatory benefits
of focusing on the inherited representations that are carried by factors in
class C3. The three reasons discussed in section 5.2 above amount to a
strong argument that formulating DST’s thesis in informational terms is
explanatorily superior and better captures the spirit of the DST project.

7. Conclusion. Developmental systems theory has championed a research
programme focused on investigating the developmental and evolutionary
importance of factors other than genes. That insight has been vindicated
by the recent flowering of empirical work in the field. However, DST’s
distinctive contribution has not been brought sharply into focus. This
article has argued that a detachable part of the DST canon—a philosophy
of nature that rejects any appeal to semantic information—has obscured
its central insight. DST’s claim is not just that nongenetic factors are
causally important. Formulated as a claim about inherited representa-
tions, DST turns into the striking thesis that some factors other than
genes also carry genuinely semantic information, in a restricted and rather
special way. If that is right, then there is a strong sense in which there
are nongenetic channels of inheritance. The payoff is that we can use
information as a common currency to compare inheritance systems and
to understand how information generated by the process of natural se-
lection is relied on to guide development toward adaptive phenotypes.

REFERENCES

Alberts, B., et al. 2004. Essential Cell Biology. 2nd ed. New York: Garland Science.
Avital, Eytan, and Eva Jablonka. 2000. Animal Traditions: Behavioural Inheritance in Evo-

lution. Cambridge: Cambridge University Press.
Bergstrom, Carl T., and Martin Rosvall. Forthcoming. “The Transmission Sense of Infor-

mation.” Biology and Philosophy.
Dretske, Fred. 1981. Knowledge and the Flow of Information. Cambridge, MA: MIT Press.
Freeland, S. J., and L. D. Hurst. 1998. “The Genetic Code Is One in a Million.” Journal

of Molecular Evolution 47:238–48.
Galloway, L. F., and J. R. Etterson. 2007. “Transgenerational Plasticity Is Adaptive in the

Wild.” Science 318:1134–36.
Godfrey-Smith, Peter. 1999. “Genes and Codes: Lessons from the Philosophy of Mind.” In

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


DST AND INHERITED REPRESENTATIONS 81

Where Biology Meets Psychology: Philosophical Essays, ed. V. Hardcastle. Cambridge,
MA: MIT Press.

———. 2000. “On the Theoretical Role of ‘Genetic Coding.’” Philosophy of Science 67:26–
44.

———. 2001. “On the Status and Explanatory Structure of Developmental Systems Theory.”
In Cycles of Contingency: Developmental Systems and Evolution, ed. Susan Oyama, Paul
E. Griffiths, and Russell D. Gray. Cambridge, MA: MIT Press.

———. 2006. “Information in Biology.” In The Cambridge Companion to the Philosophy of
Biology, ed. D. Hull. Cambridge: Cambridge University Press.

———. 2007. “Conditions for Evolution by Natural Selection.” Journal of Philosophy 54
(10): 489–516.

Gray, Russell D. 2001. “Selfish Genes or Developmental Systems?” In Thinking about Evo-
lution: Historical, Philosophical and Political Perspectives, ed. R. S. Singh, B. K. Costas,
D. B. Paul, and J. Beatty, 184–207. Cambridge: Cambridge University Press.

Griffiths, Paul E. 2001. “Genetic Information: A Metaphor in Search of a Theory.” Phi-
losophy of Science 68:394–412.

———. 2005. “The Fearless Vampire Conservator: Philip Kitcher, Genetic Determinism
and the Informational Gene.” In Genes in Development: Re-reading the Molecular Par-
adigm, ed. E. M. Neumann-Held and C. Rehmann-Sutter. Durham, NC: Duke Uni-
versity Press.

Griffiths, Paul E., and Russell D. Gray. 1994. “Developmental Systems and Evolutionary
Explanations.” Journal of Philosophy 91:277–304.

———. 1997. “Replicator II: Judgement Day.” Biology and Philosophy 12:471–92.
———. 2005. “Discussion: Three Ways to Misunderstand Developmental Systems Theory.”

Biology and Philosophy 20:417–25.
Griffiths, Paul E., and Robin D. Knight. 1998. “What Is the Developmentalist Challenge?”

Philosophy of Science 65:253–58.
Haig, D., and L. D. Hurst. 1991. “A Quantitative Measure of Error Minimization in the

Genetic Code.” Journal of Molecular Evolution 33:412–17.
Immelmann, K. 1975. “Ecological Significance of Imprinting and Early Learning.” Annual

Review of Ecology and Systematics 6:15–37.
Jablonka, Eva. 2002. “Information: Its Interpretation, Its Inheritance, and Its Sharing.”

Philosophy of Science 69:578–605.
Jablonka, Eva, and Marion J. Lamb. 1995. Epigenetic Inheritance and Evolution: The La-

marckian Dimension. Oxford: Oxford University Press.
———. 2005. Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic

Variation in the History of Life. Cambridge, MA: MIT Press.
———. 2007. “Précis of Evolution in Four Dimensions.” Behavioral and Brain Sciences 30:

353–92.
Jablonka, Eva, and Gal Raz. 2009. “Transgenerational Epigenetic Inheritance: Prevalence,

Mechanisms, and Implications for the Study of Heredity and Evolution.” Quarterly
Review of Biology 84 (2): 131–76.

Lambourn, W. A. 1930. “The Remarkable Adaptation by which a Dipterous Pupa (Taban-
idae) Is Preserved from the Dangers of Fissures in Drying Mud.” Proceedings of the
Royal Society of London B 106:83–87.

Leimar, O., P. Hammerstein, and T. J. M. Van Dooren. 2006. “A New Perspective on
Developmental Plasticity and the Principles of Adaptive Morph Determination.” Amer-
ican Naturalist 167:367–76.

Levy, Arnon. 2010. “Information in Biology: A Fictionalist Account.” Nous, doi: 10.1111/
j.1468-0068.2010.00792.x.

Lewontin, Richard C. 1974. “The Analysis of Variance and the Analysis of Causes.” Amer-
ican Journal of Human Genetics 26:400–411.

———. 1982. “Organism and Environment.” In Learning, Development, Culture, ed. H.
Plotkin, 151–70. New York: Wiley.

———. 1983. “The Organism as the Subject and Object of Evolution.” Scientia 118:65–82.
Lorenz, K. 1965. Evolution and Modification of Behavior. Chicago: University of Chicago

Press.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp


82 NICHOLAS SHEA

Mameli, Matteo. 2004. “Nongenetic Selection and Nongenetic Inheritance.” British Journal
for the Philosophy of Science 55:35–71.

Maynard Smith, John. 2000. “The Concept of Information in Biology.” Philosophy of Science
67:177–94.

Maynard Smith, John, and Erös Szathmáry. 1995. The Major Transitions in Evolution.
Oxford: Freeman.

Meaney, M. J. 2001. “Maternal Care, Gene Expression, and the Transmission of Individual
Differences in Stress Reactivity across Generations.” Annual Review Neuroscience 24:
1161–92.

Millikan, Ruth Garrett. 1984. Language, Thought and Other Biological Categories. Cam-
bridge, MA: MIT Press.

Moss, L. 2001. “Deconstructing the Gene and Reconstructing Molecular Developmental
Systems.” In Cycles of Contingency: Developmental Systems and Evolution, ed. Susan
Oyama, Paul E. Griffiths, and Russell D. Gray. Cambridge, MA: MIT Press.

Oyama, Susan. 1985. The Ontogeny of Information: Developmental Systems and Evolution.
Cambridge: Cambridge University Press.

Shannon, C. E. 1949. “The Mathematical Theory of Communication.” In The Mathematical
Theory of Communication, ed. C. E. Shannon and W. Weaver. Urbana: University of
Illinois Press.

Shea, Nicholas. 2007. “Representation in the Genome, and in Other Inheritance Systems.”
Biology and Philosophy 22:313–31.

———. 2009. “Imitation as an Inheritance System.” Philosophical Transactions of the Royal
Society B 364:2429–43.

———. Forthcoming. “Inherited Representations Are Read in Development.” British Jour-
nal for the Philosophy of Science.

———. Forthcoming. “Two Modes of Transgenerational Information Transmission.” In
Signaling, Commitment, and Emotion, ed. Brett Calcott, Richard Joyce, and Kim Ster-
enly. Cambridge, MA: MIT Press.

Stegmann, Ulrich E. 2005. “Genetic Information as Instructional Content.” Philosophy of
Science 72 (3): 425–43.

Sterelny, Kim. 2001. “Niche Construction, Developmental Systems and the Extended Rep-
licator.” In Cycles of Contingency: Developmental Systems and Evolution, ed. Susan
Oyama, Paul E. Griffiths, and Russell D. Gray, 333–50. Cambridge, MA: MIT Press.

———. 2004. “Sybiosis, Evolvability and Modularity.” In Modularity in Development and
Evolution, ed. Gerhard Schlosser and Günter Wagner. Chicago: University of Chicago
Press.

Sterelny, Kim, and Philip Kitcher. 1988. “The Return of the Gene.” Journal of Philosophy
85:339–61.

Sterelny, Kim, K. C. Smith, and M. Dickison. 1996. “The Extended Replicator.” Biology
and Philosophy 11:377–403.

Sultan, S. E. 2000. “Phenotypic Plasticity for Plant Development, Function and Life His-
tory.” Trends in Plant Science 5:537–42.

Weber, M. 2005. Philosophy of Experimental Biology. Cambridge: Cambridge University
Press.

Whiten, Andrew, N. McGuigan, S. Marshall-Pescini, and L. M. Hopper. 2009. “Emulation,
Imitation, Overimitation and the Scope of Culture for Child and Chimpanzee.” Phil-
osophical Transactions of the Royal Society B 364:2417–28.

This content downloaded from 163.1.203.198 on Mon, 8 Jul 2013 07:31:04 AM
All use subject to JSTOR Terms and Conditions

http://www.jstor.org/page/info/about/policies/terms.jsp