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6
The Baldwin effect and genetic assimilation: contrasting
explanatory foci and gene concepts in two approaches to an
evolutionary process
Paul E. Griffiths
1
The Papineau Effect
David Papineau (2003; 2005) has discussed the relationship between social learning and the
family of postulated evolutionary processes that includes ‘organic selection’, ‘coincident
selection’, ‘autonomisation’, ‘the Baldwin effect’ and ‘genetic assimilation’. In all these
processes a trait which initially develops in the members of a population as a result of some
interaction with the environment comes to develop without that interaction in their descendants.
It is uncontroversial that the development of an identical phenotypic trait might depend on an
interaction with the environment in one population and not in another. For example, some
species of passerine songbirds require exposure to species-typical songs in order to reproduce
those songs whilst others do not. Hence we can envisage a species beginning with one type of
developmental pathway and evolving the other type. If, however, the successive evolution of
these two developmental pathways were a mere coincidence, selection first favoring the ability to
acquire the trait and later, quite independently, favoring the ability to develop it autonomously,
then this would not be a distinctive kind of evolutionary process, but merely two standard
instances of natural selection. George Gaylord Simpson pointed this out in the paper that gave us
the term ‘Baldwin effect’ (Simpson, 1953). The real interest of the Baldwin effect and its
relatives lies in the mechanisms which might link the evolution of the two developmental
pathways, so that acquiring the trait through interaction with the environment makes it more
likely that later generations will evolve the ability to acquire the same trait without that
interaction.
Papineau focuses on the way in which social learning can facilitate such Baldwin-like
links. His basic idea is that the genes which accelerate the social learning of some complex
behaviour might become advantageous only if that behaviour is already being passed on by
learning in an ‘animal culture’. In this scenario the relevant genes would be selected once the
1
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
population is socially transmitting the behaviour, but not otherwise, thus yielding a scenario that
satisfies the specifications of the Baldwin effect. Papineau subjects this sort of process to closer
analysis, showing that it simultaneously exemplifies two different kinds of mechanism that the
literature recognizes as possible sources of Baldwin effects. First, there is the process that
Papineau calls ‘genetic assimilation’. Here the focus is on some complex adaptive behaviour,
potentially under the control of a suite of genes at different loci. The challenge is to explain how
this suite can get selected in virtue of their collectively producing the complex adaptive behavior.
Prima facie, it seems that the whole suite of genetic changes would need to occur
simultaneously. An answer becomes available if the complex behaviour is also learnable, for
then each gene can be advantageous on its own, in virtue of making the rest of the behaviour
more quickly or more reliably learnable. The cumulative selection of the whole suite of genes
thus qualifies as a Baldwin effect because it depends essentially on intermediate stages in which
(most of) the behaviour is learned.
This is one part of what Papineau thinks occurs in social learning cases. But he observes
that there is a yet further sense in which such cases fit the Baldwin requirements. The process he
calls ‘genetic assimilation’ takes it as given that the complex behaviour at issue is indeed
learnable. But in many cases it will be puzzling in itself that some complex behaviour can be
learned, at least insofar as instrumental learning is supposed do the work, and reward only
accrues once the whole behaviour is in place. This is where social learning plays its role: if the
behaviour is present in the ‘animal culture’, then this in itself can render it learnable and so
‘genetically assimilable’. This now gives us a second sense in which Papineau’s social learning
cases are Baldwin effects: the behaviour is only individually-learnable-and-so-geneticallyassimilable because it is already present as a learned behaviour in the animal culture.
Papineau suggests that this sort of double-strength Baldwin effect will exert powerful
selection pressures in species that exhibit a high degree of social learning. This is an interesting
empirical conjecture that may or may not prove correct. For my part, I am happy to agree that
social learning can play a role in a distinctive form of ‘niche-construction’ (Odling-Smee et al.,
2003) that can alter selective pressures in the way Papineau suggests.
I shall say nothing more here about social learning. Rather I want to focus on Papineau’s
discussion of ‘genetic assimilation’. This term was introduced by Conrad H. Waddington to refer
to a specific process (Waddington, 1942, 1953). Waddington’s process stands out among the
other ideas listed above (‘organic selection’, ‘coincident selection’, ‘autonomisation’, ‘the
2
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
Baldwin effect’) both because Waddington was able to demonstrate it in laboratory selection
experiments and because it was part of his larger vision of the relationship between development
and evolution, a vision that has influenced contemporary work in evolutionary developmental
biology or ‘evo-devo’.
Let us look more closely at the way Papineau defines “Waddington’s Genetic
Assimilation”. He says:
Suppose 5 sub-traits, say, are individually necessary and jointly sufficient for T.
Each can either be genetically fixed or acquired through (not necessarily social)
learning. (So for sub-trait TK we have allele KG which genetically fixes TK and
allele KL which allows it to be learned.)
Suppose also that at first the KGs are rare. Still, those lucky organisms that
have some TKs genetically fixed by KGs will find it easier to learn the rest of T,
and so will be favoured by natural selection (assuming that learning is here
costly). Selection will thus cumulatively build up the genes K G which genetically
fix T.
(Papineau, 2003)
This process has little connection with the one described by Waddington himself1. In
itself this is neither particularly important nor particularly surprising. Many different processes
have been proposed that might free traits from their developmental dependence on some aspect
of the environment, and terms like ‘Baldwin effect’ and ‘genetic assimilation’ have been used in
numerous senses in this extensive literature (See e.g. Belew and Mitchell, 1996; Weber and
Depew, 2003). In fact, despite calling the process ‘Waddington’s genetic assimilation’ Papineau
does not cite Waddington’s work as a source, but instead cites a well-known computer
simulation of the interaction between learning and inheritance (Hinton and Nowlan, 1996). The
interesting point is that Waddington’s actual model of genetic assimilation is simply not
1
It does resemble one version of ‘organic selection’. Patrick Bateson has argued that many learning processes have
components which might separately become independent of the environmental conditions originally required for
their development and that the efficiency and/or reliability of the learning process might thereby be improved.
Like Papineau, he points out that these variations would only be selected if organisms regularly undergo the
complete learning process (Bateson 2004, 289).
3
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
accessible to anyone who conceptualises genes in the way Papineau does in the passage quoted
above. Several recent authors have stressed the need for biologists and philosophers of biology to
become more self-conscious about the existence of multiple gene concepts and of the appropriate
range of theoretical and experimental contexts in which those concepts should be deployed
(Moss, 2002; Falk, 2000; Stotz et al., 2004; Griffiths and Neumann-Held, 1999). I will argue
here that paying attention to gene concepts helps one to distinguish two radically different
approaches to explaining how the development of a phenotypic trait can become independent of
certain aspects of the developmental environment. One approach looks to selection to forge a
link between the successive evolution of two developmental pathways to the same trait. The
other approach, represented by Waddington’s genetic assimilation, looks to developmental
biology. This latter approach seeks to explain how the development of a phenotypic trait can
become independent of an environmental stimulus (or become dependent on that stimulus) by
showing that in certain kinds of developmental systems such transitions can be produced by
small genetic changes–changes that are likely to occur spontaneously in a relatively short time.
In the first approach the explanatory focus is on the relative selective advantage of the two
developmental pathways. In the second approach the explanatory focus is on the developmental
mechanisms that make suitable variants available for selection.
2
Genetic assimilation and Gene-P
In the passage quoted above Papineau employs a concept of the gene which Lenny Moss has
labeled ‘Gene-P’:
Gene-P is defined by its relationship to a phenotype. …Gene-P is the expression
of a kind of instrumental preformationism (thus the “P”). When one speaks of a
gene in the sense of Gene-P one simply speaks as if it causes the phenotype. A
gene for blue eyes is a Gene-P. What makes it count as a gene for blue eyes is not
any definite molecular sequence (after all, it is the absence of a sequence based
resource that matters here) nor any knowledge of the developmental pathway that
leads to blue eyes (to which the "gene for blue eyes" makes a negligible
contribution at most), but only the ability to track the transmission of this gene as
a predictor of blue eyes. Thus far Gene-P sounds purely classical, that is,
Mendelian as opposed to molecular. But a molecular entity can be treated as a
4
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
Gene-P as well. BRCA1, the gene for breast cancer, is a Gene-P, as is the gene for
cystic fibrosis, even though in both cases phenotypic probabilities based upon
pedigrees have become supplanted by probabilities based upon molecular probes.
(Moss, 2001, p. 87-88)
Papineau’s five genes are Gene-Ps, each defined by a specific part (‘sub-trait’) of the
phenotypic trait T. I take it that these parts are dispositions to acquire behavioral modifications
which together amount to a disposition to acquire the new behavior T. The process he labels
‘genetic assimilation’ is therefore simply the spread of certain of these phenotypic traits as a
result of selection. His trait KG is selectively superior to KL because KG individuals acquire T
more reliably than KL individuals. The sought-for link between individuals initially learning the
sub-trait K and later individuals possessing K without learning is mediated by a process of niche
construction – a change in the selective regime as a result of behavior. In contrast, Waddington
thought that the link between the ability to reliably acquire an adaptive trait and the appearance
of individuals with an intrinsic tendency to exhibit that trait was forged by the typical nature of
the development pathways underlying adaptively valuable traits. It was for this reason that he
objected to Simpson’s term ‘Baldwin effect’ with its implication that this evolutionary process is
a special case. Waddington intended genetic assimilation to be a ubiquitous feature of phenotypic
evolution:
Simpson comes to the conclusion that the Baldwin effect, in the sense he
describes it, has probably played a rather small role in evolution. The genetic
assimilation mechanism, however, must be a factor in all natural selection, since
the properties with which that process is concerned are always phenotypic;
properties, that is, which are the products of genotypes interacting with
environments.
(Waddington, 1953, p. 386)
According to Waddington the tendency of phenotypes to become genetically assimilated
reflects the fact that there is little difference between the actual developmental processes that
underlie a highly canalised phenotype that depends on an environmental stimulus and one that
has been rendered independent of that stimulus, as I will now try to explain.
5
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
3
Genetic assimilation and Gene-D
Waddington was aware that his vision of development required a conception of the gene which
does not intrinsically link genes and specific phenotypic outcome. He made this point in ‘The
Evolution of Developmental Systems’, an address delivered in Brisbane in 1951:
Some centuries ago, biologists held what are called “preformationist” theories of
development. They believed that all the characters of the adult were present in the
newly fertilized egg, but packed into such a small space that they could not be
distinguished with the instruments then available. If we merely consider each
gene as a determinant for some definite character in the adult (as when we speak
loosely of the ‘gene for blue eyes, or for fair hair’), then the modern theory may
appear to be merely a new-fangled version of the old idea. But in the meantime,
the embryologists, who are concerned with the direct study of development, have
reached a quite different picture of it … This is the theory known as epigenesis,
which claims that the characters of the adult do not exist already in the newly
fertilized germ, but on the contrary arise gradually through a series of causal
interactions between the comparatively simple elements of which the egg is
initially composed. There can be no doubt nowadays that this epigenetic point of
view is correct.
(Waddington, 1952, p. 155)
In Waddington’s vision of development, the entire collection of genes makes up a
developmental system which produces a phenotype. Many features of the phenotype are
explained by the dynamical properties of that developmental system as a whole, rather than by
the influence of one or a few specific alleles. Thus, for example, Waddington sought to explain
one of the major biological discoveries of his day–the fact that extreme phenotypic uniformity
can be observed in many wild populations despite extensive genetic variation in those same
populations–by appealing to the global dynamics of developmental systems. A ‘canalised’
developmental system takes development to the same endpoint from many different genetic
starting points. The development of wild-type phenotypes can thus be buffered against genetic
6
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
variation. Waddington represented this idea with his famous ‘developmental landscape’ (Figure
1).
7
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
Figure 1. Waddington's ‘ developmental landscape’. (a) The developmental trajectory of
the organism, represented by the rolling ball, is determined by a landscape representing the
developmental dynamics of the organism. (b) The shape of this landscape is determined by
genes, here represented by pegs pulling the landscape into shape via strings, and by epistatic
interactions between genes, here represented by connections between strings. From Waddington
(1957: 36).2
2
Note to editor: Copyright request to: Allen & Unwin Ltd., 19 Crompton Terrace, London, N1
2UN, for pg.36 of 'The Strategy of the Genes - A Discussion of Some Aspects of Theoretical
Biology'; C.H. Waddington; Ruskin House (copyright George Allen & Unwin Ltd.); 1957.
8
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
In modern terms, Waddington’s ‘developmental landscape’ is a representation of
development as complex system whose parameters are genetic loci and whose state space is a set
of phenotypic states. The state space is depicted as a surface, each point of which represents a
phenotype. The genetic parameters are depicted as pegs that pull on the surface and thus
determine its contours. Epistatic interactions between loci are represented by links between the
cords by which those loci pull on the surface. The development of an organism over time is
represented by the movement of a ball over the surface, which is dictated by gravity, so that the
ball rolls downhill on a path dictated by the contours of the surface. The development of the
organism is thus represented by its trajectory over the surface, through successive phenotypic
states. The basic point which Waddington uses this representation to make is that if the surface
has any significant contours, then the effect of a change at one genetic locus will be dictated by
the overall shape of the landscape, which is a global consequence of the states of all the other
genetic loci. Some genetic changes, such as those which affect the tops of inaccessible ‘hills,’
will have no effect on development. Other changes of the same intrinsic genomic magnitude
which affect the entrance of a valley or ‘canal’ will have a massive effect on development. The
phenotypic impact of a genetic change is not proportional to the magnitude of the genomic
change, but depends on the overall dynamics of development. Furthermore, the phenotypic
difference produced by a genetic difference is not explained by that genetic difference in itself,
but by how that change interacts with the rest of the developmental system. This picture retains
considerably validity in the light of contemporary developmental genetics (Gilbert, Opitz, and
Raff, 1996; Wilkin, 2003)
Thus, in Waddington’s vision, phenotypes are global expressions of genomes, but it does
not follow that particular parts of the phenotype express particular parts of that genome. The
gene concept that fits this thoroughly epigenetic view of development is the one which Moss has
labeled ‘Gene-D’:
Quite unlike Gene-P, Gene-D is defined by its molecular sequence. A Gene-D is a
developmental resource (hence the “D”) which in itself is indeterminate with
respect to phenotype. …To be a gene for N-CAM, the so-called “neural cell
adhesion molecule,” for example, is to contain the specific nucleic acid sequences
from which any of a hundred potentially different isoforms of the N-CAM protein
may potentially be derived …N-CAM molecules are (despite the name) expressed
9
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
in many tissues , at different developmental stages, and in many different forms.
The phenotypes of which N-CAM molecules are co-constitutive are thus highly
variable, contingent upon the larger context, and not germane to the status of NCAM as a Gene-D.
(Moss, 2001, p. 88, emphases in original)3
To understand Waddington’s vision of development it is essential not to think of genes as
‘genes for’ particular phenotypes or phenotypic differences (Gene-P), but instead to think of
them as parameters of a developmental system (Gene-D). It is necessary to think in terms of
what in Waddington’s day was known as ‘physiological genetics’.
In a series of widely-read papers the philosopher Andre Ariew has used Waddington’s
concept of canalisation to explicate the concept of innateness (Ariew, 1996, 1999). Innate traits,
Ariew has argued, are those traits insensitive to environmental variation, or, equivalently, those
traits which are canalised with respect to changes in the environmental parameters of a
developmental system. Unfortunately, Ariew’s work has led philosophers who know of
Waddington only through these papers to use the term ‘canalisation’ and even ‘genetic
canalisation’ to mean insensitivity to environmental variation. In fact, the idea of insensitivity to
environmental factors, properly known as ‘environmental canalisation’ (Wagner, Booth, and
Homayoun, 1997), cannot even be represented in Waddington classic picture of the
developmental landscape (Figure 1). Environmental parameters are not included in this model,
and whether a phenotype is canalised in Waddington’s original sense is a question of the
dynamical structure of the developmental system, not the relative role of genes and
environment.4 But the model can easily be extended to include environmental parameters, and
Waddington himself does so when discussing genetic assimilation, as seen below. If these
additional parameters are added, then we can define both ‘environmental canalisation’ and
‘genetic canalisation’. A phenotypic outcome is environmentally canalised if those features of
3
Philosophers will note that Gene-P and Gene-D correspond respectively to ‘descriptive’ and ‘rigid’ readings of the
phrase ‘the gene for T’ when this phrase is used in the usual way to report the fact that some DNA sequence
accounts for a large portion of the variance in trait T in some study population (See Sterelny and Griffiths, 1999, p.
90-92).
4
The evolutionary developmental biologist Brian Hall has written extensively on Waddington and has stressed that
his thought was profoundly ‘gene centered’ in the sense that he saw the developmental system as primarily and
predominantly the expression of a potential present in the genome (Hall, 2003, 1992, 1999).
10
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
the surface which direct development to that endpoint are relatively insensitive to the
manipulation of environmental parameters. A phenotypic outcome is genetically canalised if
those features of the surface which direct development to that endpoint are relatively insensitive
to the manipulation of genetic parameters. It should be noted, however, that we are not forced to
draw this distinction. The idea of canalisation with respect to all the parameters that are included
in a model of the developmental system is equally legitimate. It is, after all, far from clear
whether to classify many critical parameters, such as the presence of DNA methylation or of
maternal gene products in the cytoplasm, as ‘genetic’ or ‘environmental’. The issue of genes
versus environment is peripheral to Waddington’s central concern, which is how developmental
outcomes can be robust and reliable in the face of variations in developmental parameters.
Like some modern authors, Waddington believed that natural selection would favor the
canalisation of important adaptive phenotypes. Developmental systems that produce important
adaptive outcomes robustly will be selected over those that are easily perturbed. Although I do
not have time to explore this theme fully here, it is important to recall that, like his
contemporaries I.I Schmalhausen and Theodosius Dobzhansky, Waddington saw natural
selection as optimizing, not the phenotypic character itself, but rather a norm of reaction which
specifies a range of phenotypes as a function of genetic backgrounds and environmental
conditions: “An animal is, in fact, a developmental system, and it is these systems, not the mere
static adult forms which we conventionally take as typical of the species, which become
modified in the course of evolution” (Waddington, 1952, 155). When there is a single, optimal
phenotype, ‘stabilising selection’ will operate to select a narrow reaction norm, or, in other
words, to canalize the phenotype. In other circumstances, however, selection may favour a
broader reaction norm, producing what we describe today as ‘adaptive phenotypic plasticity’.
The shape of the norm of reaction is itself a character produced by natural selection.
We are now in a position to see why Waddington thought there would be little difference
between the actual developmental processes that underlie a highly canalised phenotype that
depends on an environmental stimulus and those that underlie one that has been rendered
independent of that stimulus. Waddington writes:
If natural selection was in this way acting in favour of the ability to respond in a
useful way to some environmental stimulus, it would also in time build up a
canalised response, so that the most valuable degree of expression was regularly
11
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
achieved. Once that had been done, the genotype would have been modified so
that it determined a new valley on the developmental surface; but it would still
require the push of an environmental stimulus to cause one of the balls in our
model to run into it. However, once the valley was formed and canalised, the
exact strength of the push, and the exact time at which it was applied, would be of
lesser importance. In fact, we might expect that, by this stage in the evolution
[sic], there would be a number of mutant genes available in the species which
could divert development into the prepared channel; and thus, once the ground
had been prepared, as it were, an internal genetic mechanism could take over from
the original environmental stimulus. We can thus envisage a mechanism by which
a valuable response to the environment could become gradually incorporated into
the hereditary endowment of the species.
(Waddington, 1952, p. 159)
I have discussed elsewhere how some of Waddington’s contemporaries, particularly
J.B.S Haldane and his wife and collaborator Helen Spurway, saw his work on genetic
assimilation as demonstrating that there need be little difference as regards developmental
genetics between ‘innate’ and ‘acquired’ traits (Griffiths, 2004). Haldane and Spurway drew on
Waddington to argue that transitions back and forth between instinct and learning were to be
expected in response to the adaptive advantages of these two forms of development in specific
environments. A couple of brief quotations will give the flavour of this work:
[discussing passerine song learning] some of these species must have passed
through a stage where the song was learnt by some individuals and was instinctive
in others. As a geneticist I think that it is quite impossible to make a sharp
distinction between learnt and unlearnt behavior.
(Haldane, 1992 [1955], p. 605).
The number of generations during which a learned ethogenesis evolves into an
instinctive ethogenesis, if it does so at all, depends on the relative strength of the
selection pressures favouring uniformity and variability in development.
(Haldane and Spurway, 1954, p. 275)
12
In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
One of the most exciting features of this, Waddingtonian, vision of transitions between
instinct and learning is its symmetry. Most accounts of the Baldwin effect and its relatives focus
exclusively on the elimination of dependence on an environmental factor, but the mechanisms
underlying Waddington’s genetic assimilation can equally lead to ‘environmental assimilation’
when the selection pressures are reversed. ‘Baldwinian’ phenomena are thus subsumed under the
more general topic of the selective advantages of different patterns of interaction between gene
and environment–the field of research known today as ‘adaptive phenotypic plasticity’
(Brakefield and Wijngaarden, 2003; Schlichting, 2003). The traditional emphasis on the Baldwin
effects and its relatives to the exclusion of other evolutionary patterns reflects a misguided desire
to get the effects of the environment on development ‘written into the germline’, which in turn
reflects the mistaken conviction that only in this way can the effects of the environment on
development be of evolutionary significance (Griffiths, 2003).
4
Gene concepts and explanatory foci
In the evolutionary scenario described by Papineau the gene for trait K (‘allele K G’) spreads
through the population in response to a selection pressure caused by the spread of a learnt trait T
whose acquisition requires five separate dispositions each of which corresponds to a gene (‘allele
KL’ and four companions). As I remarked above, these genes are Gene-Ps – they are DNA
elements individuated by the criteria that their presence is a reliable statistical predictor of a
phenotypic difference. This, I suggest, is typical of one way of thinking about how the
development of a phenotypic trait can become independent of certain aspects of the
developmental environment. The evolutionary problem is framed as follows: 1) What are the
adaptive advantages of having T conditional on an environmental factor? 2) What are the
adaptive advantages of having T independent of that factor? 3) Does the evolution of the first
trait produce new selection pressures which favour the evolution of the second? The genes that
feature in typical scenarios designed to address these questions are Gene-Ps corresponding to the
difference between the first trait and the second.
In contrast, most of the genes that figure in Waddington’s genetic assimilation scenario –
the ‘pegs’ in Figure 1 – are genes that are present both when the trait is dependent on the
environment and when it is independent of the environment. They are the genes (Gene-Ds)
which play a causal role in building the K phenotype, not the genes that differ between cases
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In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
Oxford: Oxford University Press, 2006: 91-101.
where that particular cascade of gene expression is switched on endogenously and cases where it
is switched on exogenously or even the genes that differ between individuals that have K and
those that lack K. The evolutionary problem is framed as follows: How does evolution produce
traits which can be readily switched between different triggers? This second way of thinking
about how the development of a phenotypic trait can become independent of certain aspects of
the developmental environment corresponds to some of major themes in recent evolutionary
developmental biology, namely the evolution of developmental modularity (Gass and Bolker,
2003; Wagner, 2001) and the evolution of phenotypic plasticity (Preston and Pigliucci, 2004;
Gilbert, 2001; Brakefield and Wijngaarden, 2003). These evolutionary problems simply cannot
be posed if evolution is represented as change over time in the frequency of ‘genes for’ specific
phenotypes (Gene-Ps).
We can compare these two ways of thinking about how the development of a phenotypic
trait can become independent of certain aspects of the environment with two ways to approach
the evolution of sexual differentiation. The primate SRY gene on the Y chromosome is a Gene-P
with respect to the masculinisation of the foetus: individuals who have this gene are very likely
to have a male phenotype. But it does not follow that the evolution of sexual differentiation
should be studied by asking how the SRY gene evolved. The masculinisation of the mammalian
foetus is the result of a complex cascade of a gene expression. Both male and female foetuses
have almost all the genes involved in this cascade. In Waddington’s terms the developmental
landscape has a deep branching valley running across it and the SRY gene, or its equivalent in
other mammals, simply nudges the foetus into one branch rather than the other. With this picture
in mind, it is easy to understand how two rodents of the genus Ellobius have managed to lose the
whole Y chromosome whilst retaining the gene expression cascade of mammalian sexual
development. Some other gene expression event early in development acts to triggers the same
cascade. Furthermore, sexual differentiation is an ancient characteristic of vertebrates and in this
larger group cascades of gene expression that are to some degree homologous with those in
mammals are triggered in still more diverse ways. Crocodiles, amongst others, have
environmentally triggered sexual differentiation. Some fish retain the capacity for females to be
masculinised by an environmental trigger throughout their life cycle. From the viewpoint of
developmental genetics, understanding the evolution of the specific triggering cause in one group
or another is not the way to understand the evolution of the cascade of gene expression which
constitutes becoming male. Nevertheless, there is nothing wrong with Gene-P thinking in the
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In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition.
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right context–if we want to ask about the evolutionary pressures leading to genetic versus
environmental sex determination it is appropriate to pose the question in terms of the selection
pressures on the specific loci involved in these two modes of triggering. In the same way, we can
examine the selection pressures on the specific loci involved in making the switch between the
dependence of a behavior on learning and its independence of learning, as Papineau does, but
this should not be confused with the quite different project in which Waddington was engaged,
namely asking how developmental systems make such options readily available to selection.
5
Conclusion
Many evolutionary processes have been described in which a trait that initially develops in the
members of a population as a result of some interaction with the environment comes to develop
without that interaction in their descendants. Waddington’s genetic assimilation is importantly
different from the rest of this ‘Baldwiniana’ because his explanatory focus was not on the
selection pressures at the point of transition, but on how developmental systems come to be
structured in such a way that these evolutionary transitions are readily accessible to evolving
lineages. Waddington’s approach also replaces the simple contrast between ‘acquired’ and
‘innate’ with a non-dichotomous model of developmental canalisation and phenotypic plasticity
that is in line with recent work on the evolution of development. From a Waddingtonian
perspective evolutionary transitions between ‘innate’ and ‘acquired’ are only to be expected
because those categories have little meaning in terms of developmental genetics and in some
cases the difference between the ‘innate’ and ‘acquired’ may require only a minimal change in
developmental mechanisms. But to see this it is necessary to use a gene concept suitable for
thinking about development, and not a gene concept designed for theoretical population genetics
or for the prediction of phenotypic differences within populations.
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