Biology and Philosophy (2005) 20:11–20

DOI 10.1007/s10539-004-1605-0
Springer 2005

-1
Review

Review of ‘Niche Construction’1

PAUL E. GRIFFITHS*
Department of History and Philosophy of Science
University of Pittsburgh
Pittsburgh
PA 15206
USA

Research on the effects of niche construction is one of the most exciting recent
developments in evolutionary theory. The idea that organisms shape their
environments as well as being shaped by them is familiar to many philosophers
from two famous papers by Richard Lewontin from the early 1980s (Lewontin
1982, 1983). There is a deal of difference, however, between a challenge to
orthodox evolutionary theory, however compelling, and a substantial program
of research that can claim to have expanded evolutionary theory so as to meet
that challenge. In numerous publications over the last decade and a half the
three authors of this work have succeeded in giving real substance to the idea of
niche construction by embodying it in a series of population genetic models
and demonstrating its potential effect on evolutionary dynamics.
Niche construction is a challenge to what Lewontin called the ‘lock and key’
model of adaptation. In this metaphoric vision of evolution the adaptations of
organisms are solutions (keys) to the problems posed by the environment
(locks). Organisms are adapted to their ways of life because they were made to
fit those ways of life. In place of this traditional metaphor of adaptation as ‘fit’,
Lewontin suggested a metaphor of mutual construction. Organisms and their
ecological niches are co-constructing and co-defining. Organism’s both physi-
cally shape their environments and determine which factors in the external
environment are relevant to their evolution, thus assembling such factors into
what we describe as their niche. Organisms are adapted to their ways of life
because organisms and their way of life were made for (and by) each other. For
example, beavers are well-adapted to life in the lakes which are created by their
own dams. Eucalypt forests are well-adapted to the intense fire regime that is
sustained by their own habits of growth and decay. Humans are well-adapted
to survive and reproduce in the context of human material and ideational
cultures.

*Present address: Philosophy program, SHPRC, University of Queensland, Brisbane, QLD 4072,
Australia (e-mail: pauleg@pitt.edu)
1
This review has benefited considerably from discussions with Karola Stotz and John Norton. The
discussion of thermodynamics draws on (Earman and Norton 1999a).
12

The introductory chapter of this book recalls two pairs of equations that
Lewontin used to contrast the traditional model of adaptation as ‘fit’ and the
new model of adaptation as construction. The first pair of equations express
the conventional picture. Change in organisms over time is a function of the
state of those organisms and their environment at each previous instant. The
environment acts on the existing state of organisms by selecting those best
fitted to the environment. The environment itself changes over time too, but as
the second equation shows these changes are not a function of what organisms
are doing at each previous instant.
dO=dt ¼ f(O,E) ð1Þ

dE=dt ¼ g(E) ð2Þ

Lewontin’s alternative picture is given by Eqs. (3) and (4). Organisms and
their environments play reciprocal roles in each other’s change. Change in the
environment over time is a function of the state at each previous instant of both
the environment and the organisms evolving in that environment.
dO=dt ¼ f(O,E) ð3Þ

dE=dt ¼ g(O,E) ð4Þ

The focus of this volume is on a related equation giving change over time in
an organism’s niche, the source of future selection on that lineage of organisms,
as a function of the prior states of organism and environment. Those states or
organism and environment are, of course, the outcomes of Eqs. (3) and (4).
NðtÞ ¼ h(O,E) ð5Þ
The expression N(t), the niche of the population of organisms O at time t, is
defined as the complete set of selective pressures to which that population is
exposed. This definition is an evolutionary twist on the conventional, Hutch-
insonian definition of a niche as a hyperspace whose axes represent all the
factors which must fall within some tolerance range if a species is to maintain
itself. Like the conventional Hutchinsonian niche, this ‘selective niche’ is de-
fined relative to a specific population of organisms. Physical changes in the
environment that make no difference to the selection pressures on that popu-
lation are not changes in the niche. Conversely, an event like migration need
not change the physical environment at either end of the migration but changes
the niche nevertheless. ‘‘Niche Construction occurs whenever a population O
changes its relativistic niche by changing a factor in E relative to its own
features’’ (p. 43).
Niche construction can take several more specific forms. The authors rec-
ognise the distinction just mentioned between perturbation, in which organisms
 13

physically alter the value of a niche parameter and relocation in which

organisms change the value of a niche parameter by simply moving to a spot
where it has a different value. This distinction has been the focus of earlier
philosophical discussion of niche construction (Brandon 1990; Godfrey-Smith
1996). Although relocation is not niche ‘construction’ in a literal sense, the
effect of relocation on the future evolution of a population will often be the
same as that of perturbation of the existing locale, so it makes sense to allow
evolutionary models to treat the two processes together. The authors also
distinguish inceptive niche construction, in which organisms actively perturb a
niche parameters that would otherwise be stable, from counteractive niche
construction, in which organisms stabilise niche parameters that would
otherwise be changing. Counteractive niche construction plays a major role in
later chapters of the book that discuss possible tests of the niche construction
framework. The authors argue that the failure of a population to respond to an
apparent selection pressure may indicate counteractive niche construction and
that such observations should trigger a search for constructive interactions
between the population and the relevant niche parameters. Finally, the authors
distinguish positive niche construction, which enhances the fitness of the
organism that acts on the niche from negative niche construction, which
diminishes that fitness. They thus count as ‘niche construction’ any impact
whatever of the population on its selective environment, including driving itself
to extinction by degrading its resource base.
Since the eight processes defined by combining these three distinctions are all
counted by the authors as instances of niche construction, the conception of
niche construction advocated here is a very broad one. Nevertheless, all the
niche construction processes mentioned up to this point concern the impact of
a population on its own niche. In a further extension of the concept Odling-
Smee, Laland and Feldman treat the impacts of the activity of one population
on the selective niche of any other population as another instance of niche
construction. A population of organisms that drives another population of
organisms extinct by changing a critical parameter in the environment of that
organism is thus said to be engaging in perturbative, inceptive, negative niche
construction with respect to the second population. Niche construction thus
subsumes the entire network of relationships that make up an ecosystem. The
extreme generality of this conception is intentional. One major focus of the
book is to suggest a possible unification of community ecology with process
functional ecology via the general framework of niche construction. Biota and
abiota form an ecological network in which the activities of the biotic nodes
impact on other biotic nodes in a complex dance of mutual niche construction.
Ecological impacts and selection pressures are simply different aspects of the
connectedness of this network. I am not going to pursue this important aspect
of the book directly. Instead, I want to focus on one of the sources of the
authors’ confidence that the niche-construction framework can be extended
from its initial foundations in such striking examples as beaver dams, eucalypt
fire regimes and human culture to provide a general framework for ecology and
14

evolution. The authors embed their account of biology within the still more
general framework of thermodynamics. When organisms are viewed as a dis-
tinctive kind of thermodynamic system, they argue, it becomes clear that niche
construction is a universal feature of living systems and that at the most ab-
stract level, ecological relationships can be conceived of as organisms inter-
acting thermodynamically with the environment. Most of chapter four of the
book is devoted to elucidating this idea and the results of that discussion are
appealed to regularly in later chapters. Despite this extensive treatment I do
not think that the authors succeed in establishing the implications of ther-
modynamics for biology to which they later appeal.
Odling-Smee, Laland and Feldman are not the first biologists to try to locate
biology within the more general framework of thermodynamics. The best
known attempt is probably Daniel Brooks and Edward Wiley’s Evolution as
Entropy: Toward a Unified Theory of Biology (Brooks and Wiley 1988), al-
though many other authors have made contributions in this field (Weber et al.
1988). Like most of the earlier treatments, the present authors start with the
uncontroversial claim that living systems are dissipative systems – they main-
tain a highly ordered internal state by drawing on external sources of energy
and exporting entropy into their surroundings. The authors identify this export
of entropy with niche construction and set out to give a general, thermody-
namic characterisation of niche construction: ‘some properties of niche con-
struction should be general, if only because, regardless of species, all organisms
have to live at their environments’ expense, and they can do that only by acting
on and perturbing their environments’ (p. 170). If niche construction is to
evolve, it must be profitable to the organisms that engage in it, yielding more
energy that it consumes. Organisms, they argue, are ‘Maxwell’s demons’ which
on average decrease their own entropy at the expense of their surroundings. It
follows that:
Niche construction in its interactions with natural selection must there-
fore be regulated and controlled by information. Specifically, the niche-
constructing activities of organisms must be at least partly governed by
and directed by semantic information, or knowledge, supplied by the
evolutionary process as a result of natural selection… and typically
encoded in DNA (p. 177).
While I think that an important part of this thesis can be salvaged, I will
argue here (i) that the argument from accepting this thermodynamic charac-
terisation of organisms to the conclusion that their activities must be guided by
information is much less straightforward than the authors suppose, (ii) that
semantic information is, in any case, entirely the wrong sort of information to
make the necessary connections to thermodynamics, and (iii) that locating
semantic information primarily in DNA sequence sacrifices many of the
potential insights of the niche-construction framework.
First, what does it mean to say that organisms are Maxwell’s demons?
Maxwell’s ‘demon’ is a creature who knows the positions and velocities of
 15

particles of two gases separated by a partition. The demon controls a trapdoor

in the partition which it opens and shuts so as to allow through fast moving
particles from one side and slow moving particles from the other side. This
causes an increase in the temperature of one gas at the expense of the other, in
contradiction of the second law of thermodynamics, which states that no iso-
lated thermodynamic cycle can exist whose sole effect is an increase in the
temperature of a body at the expense of a cooler body. Looked at another way,
the demon has caused a spontaneous decrease in entropy, enhancing the
orderliness of its little world without creating a matching disorder elsewhere.
The point of Maxwell’s original thought experiment is that what the demon
does deliberately, chance can also accomplish. In a vast array of chambers with
a simple hole in place of the demonically operated trapdoor, some chambers
will spontaneously depart from thermal equilibrium. That this can, and will,
happen demonstrates that the second law of thermodynamics is an irreducibly
statistical law, something that had not been universally accepted when Maxwell
wrote. Given the huge number of particles involved in any macroscopic ther-
modynamic phenomena, spontaneous decreases in entropy on this scale will be
astronomically rare and we cannot realistically expect to observe one. On a
smaller scale, however, ensembles of particles do spontaneously depart from
thermal equilibrium. They accomplish this not by all rushing to the same side
of Maxwell’s chamber, but by spontaneously bombarding observable particles
in an asymmetric fashion causing observable movement. This was Einstein’s
famous 1905 explanation of Brownian motion. The operation of Maxwell’s
demon can thus be observed through a light microscope.
It is often said that Maxwell’s demon is ‘impossible’ since it defies the second
law of thermodynamics. The example of Brownian motion shows that this is not
quite correct. What is impossible in a system that consistently defies the second
law, which is as it should be if that law is irreducibly statistical in nature. Even
more importantly, it is impossible to build a ‘perpetual motion machine of the
second kind’ – a system which consistently defies the second law and by doing so
is able to perform some physical work. Any system which appears to be a
perpetual motion machine of the second kind must in reality be drawing on
some source of external energy so that the larger system which includes that
energy source obeys the second law. So when Odling-Smee, Laland and Feld-
man assert that organisms are Maxwell’s demons, what they really mean is that
they appear to be Maxwell’s demons if one ignores the external sources of
energy upon which they draw to maintain themselves far from thermal equi-
librium. Since it is important not to confuse such systems with genuine Maxwell
Demons I will refer to them from now on as ‘Fool’s demons’.
What is the point of recognising that organisms are Fool’s demons? The
authors think it will allow them to deduce that organisms have a number of
properties that physicists have attributed to Fool’s demons:
On the assumption that far-from-equilibrium organisms can stay alive
only if they are endowed with these Maxwell’s-demon-type properties, we
16

can now go back to evolutionary biology and use this list of properties to
indicate the universal characteristics we should find in all niche-con-
structing organisms (p. 175).
According to the authors there are six of these properties. Fool’s demons,
and thus organisms, must (1) have a goal; (2) discriminate states of their
environment; (3) anticipate those states; and in order to do this must (4) be
‘instructed by knowledge’ (p. 173, their emphases), which in turn implies pos-
sessing a memory. They must (5) be designed in a way that allows them to
accomplish these things and (6) be supplied with an external source of energy.
The last two properties are uncontroversial. Six follows directly from the
second law of thermodynamics. Five is supported by all the arguments that
usually lead us to attribute complex adaptations to natural selection rather
than chance. It is perhaps also uncontroversial that any Fool’s demon must be
a goal-directed system in some broad, cybernetic sense since its operation can
be represented as an attempt to minimise some physical quantity. It is prop-
erties 2–4 about which I am sceptical. The idea that all Fool’s demons must be
information processing systems in any non-trivial sense is far from obvious.
Physicists have described many Fool’s demons. One of the earliest suggestions
was to replace Maxwell’s original demon and trapdoor with a one-way valve
delicate enough to be opened by fast moving molecules. Another involved a
nano-scale ratchet mechanism operated by Brownian motion. One recent
proposal implements something like the one-way valve using an arrangement
of velocity dependent force-fields. These systems can be described as ‘pro-
cessing information’, but only in the trivial sense that the planets ‘compute’
their course around the sun by ‘integrating’ the gravitational forces to which
they are subject. The only reason to describe them in this fanciful way would be
if it gave access to some theorems of information theory that would throw light
on why the second law of thermodynamics holds. But the well-known proofs
that any information processing system that is designed to implement a per-
petual motion machine of the second kind will be defeated by the entropic costs
of information processing are derived from the second law and not the other
way around (Earman and Norton 1999b). There is an active research program
which aims to derive the second law from an information-theoretic treatment
of thermodynamics, but the viability of that research program remains
controversial.
I have suggested that thermodynamics does not provide strong support for
the view that information processing is amongst the universal characteristics of
niche constructing organisms. But suppose that I am wrong about this. If the
present authors could show that organisms must use information to sustain
themselves far from thermal equilibrium, how could they get from there to the
view that this information is ‘‘supplied by the evolutionary process as a result
of natural selection … and typically encoded in DNA’’ (p. 177). The problem is
that, while there is an intellectually respectable way to treat genes as an
information conduit by which the effects of selection on past generations are
 17

transmitted to future generations, the relevant concept of information is quite

different from that which figures in the mathematical theory of communication
and it is only the later concept that has a formal connection to the measure-
ment of entropy and thus to thermodynamics.
According to the present authors, DNA ‘‘carr[ies] knowledge in the form of
meaningful information about phenotypes in particular environments’’
(p. 183). The idea that evolutionary adaptation is essentially a process of
knowledge acquisition has been extensively explored in the writings of Karl
Popper, Donald Campbell and Konrad Lorenz and the present treatment is
along much the same lines. Natural selection is seen as trial and error learning,
with individual lives constituting trials. The results of this process are genomes
which are passed on to future generations. The adaptive phenotypes of those
future generations are seen as reflecting information about the adaptive
requirements of the environment that those organisms have inherited from
their ancestors. This information, it is argued, must have reached the organism
via its genome since genomes are what organisms inherit from their ancestors.
It is semantic information because it is about some subject matter and because
it can misrepresent that subject matter when environmental change renders a
previously successful lineage of organisms maladapted. So, ‘‘natural selection
leaves residues of semantic information about what characters are valuable in
the environments of evolving populations, in the selected genes of organisms’’
(p. 183).
Odling-Smee, Laland and Feldman argue that it is this, semantic informa-
tion that allows organisms to maintain themselves far from thermodynamic
equilibrium. But as they themselves make clear, ‘‘a sequence of nucleotide
bases in a stretch of DNA can in principle be measured in bits, but what a gene
means cannot be so measured’’ (p. 183). The ‘knowledge’ or ‘meaningful
information’ that flows from parent to offspring is simply not the same thing as
the quantity of Shannon-information that a descendant genome carries about
an ancestral genome or the quantity of Shannon-information that a genome
carries about the selective environments of ancestral genomes. Yet it seems
reasonably clear to me that it is Shannon-information that must be the focus of
any attempt to use natural selection as the external source of order that makes
organisms Fool’s demons and not genuine (impossible) Maxwell’s demons.
This is because Shannon information will reflect the imposition of order on one
physical system by a causal connection to another physical system and, as I
discuss below, it is by this means that natural selection is able to construct
dissipative systems.
The lack of connection between semantic information and thermodynamics
is also reflected in the fact that whether a genome is rich in semantic infor-
mation has no obvious connection to whether it has high or low entropy. A
genome composed largely of trinucleotide repeats or of ‘dead’ transposons
would be highly ordered and thus have low entropy, but it would not thereby
be rich in semantic information about past environments. Conversely, a gen-
ome under strong selective constraint on genome size, leading to the
18

elimination of many duplicate genes and many repetitive non-coding regions

will be unusually incompressible and thus, in information theoretic terms, have
higher entropy than other genomes of the same length. But this is precisely
because it is more adaptively fine-tuned than most genomes, with most sur-
viving sequences having some adaptive function. So presumably, it must be
rich in semantic information. In conclusion, it seems distinctly unlikely that, if
there is a connection between the literature on information and entropy and a
thermodynamic perspective on biology, that link can be made using the notion
of semantic information, rather than one of the family of information-theoretic
notions which were inspired by the study of entropy and thus, share much of
their formal apparatus with thermodynamics.
A further concern I have with the present attempt to treat niche-construction
thermodynamically is the author’s claim that the information which organisms
use to defeat the second law of thermodynamics is contained in the organisms’
DNA. I found it puzzling that a book whose subject is the multiple causal
channels by which a parental generation can influence their descendants would
ignore the role of those very channels in the transmission of the structures
which allow organisms to defeat entropy and stay alive. DNA, after all, is not
very good at maintaining itself far from thermal equilibrium. That is why fossil
DNA offers such a frustratingly short time-horizon in paleontology. The rea-
son DNA structure can be reliably transmitted over many millions of years in
living systems is that it forms part of a metabolic system which is structured as
a dissipative system, drawing energy from its environment and using that en-
ergy to actively maintain a highly ordered internal state by, for example,
continually repairing its DNA.2 Thus, if we take on the task of explaining how
organisms can be Fool’s demons, a task that is most pressing to researchers
investigating the origins of life, what we primarily have to explain is how
organisms can pass on to their descendants the dissipative structures that keep
them far from thermal equilibrium. DNA-based heredity is only one part of
that story. Another obvious part of the story is that living systems use mem-
brane heredity to ensure that the DNA finds itself in a local (cellular) envi-
ronment that is highly ordered before the first gene product emerges from the
new nucleus. To cut the story short, the whole gamut of epigenetic inheritance
systems and multiple heredity channels (Jablonka and Szathmáry 1995) are
relevant to understanding how living systems can recreate in their offspring the
highly ordered states that constitute being alive. Moreover, all these heredity
systems are subject to natural selection and can thus be regarded as trans-
mitting semantic information derived from natural selection (Sterelny et al.
1996; Griffiths and Gray 1997; Griffiths 2001).
I have expressed puzzlement at finding a near-exclusive focus on DNA-based
heredity in a book whose subject is the multiple causal channels by which a
parental generation can influence their descendants. One explanation may be

2
Viruses are, of course, a near exception which is one reason why they are necessarily parasitic on
systems with such a metabolism.
 19

that the book’s focus is so much on how organisms construct the selective niche
of their descendants, rather that on how they construct their developmental
niche. The authors recognise that ‘‘Niche construction … contributes to both
the building of the next generation and to changes in the niche-constructing
organism’s own selective environments’’ (p. 381) and it is clear from earlier
work that they have a substantial interest in the former process. Nevertheless,
they devote only three of this book’s four hundred and seventy pages to po-
tential links between the niche-construction framework and developmental
biology. There are substantial issues that urgently need to be addressed con-
cerning the relationship between niche construction and recent work on the
ecological context of development (Gilbert 2001). Such work would rapidly
reveal the need to extend the framework of this book to include the extra-
genetic channels through which parents influence the phenotypes of their
offspring. It is indisputable that organisms recreate in their offspring the dis-
sipative structures that allow them to maintain themselves far from thermal
equilibrium. That they are able to do this owes a great deal to natural selection.
However, as Daniel Lehrman wrote many years ago, ‘‘Natural selection acts to
select genomes that, in a normal developmental environment, will guide
development into organisms with the relevant adaptive characteristics. But the
path of development from the zygote stage to the phenotypic adult is devious,
and includes many developmental processes, including, in some cases, various
aspects of experience’’ (Lehrman 1970). One lesson of niche construction re-
search is surely that those aspects of experience, as much as the genes with
which they interact, have evolutionary explanations.

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