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First published online May 26, 2006
Journal of Experimental Biology 209, 2362-2367 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02070
Review Article: Phenotypic Plasticity in Evolution |
Phenotypic plasticity and evolution by genetic assimilation
1 Department of Ecology and Evolution, SUNY-Stony Brook, 650 Life Science
Building, Stony Brook NY 11794, USA
2 Department of Biology, College of Charleston, Charleston, SC 29424,
USA
3 Department of Ecology Evolutionary Biology, University of Connecticut,
Storrs, CT 06269, USA
* Author for correspondence (e-mail: pigliucci{at}genotypbyenvironment.org)
Accepted 3 January 2006
Summary
In addition to considerable debate in the recent evolutionary literature about the limits of the Modern Synthesis of the 1930s and 1940s, there has also been theoretical and empirical interest in a variety of new and not so new concepts such as phenotypic plasticity, genetic assimilation and phenotypic accommodation. Here we consider examples of the arguments and counter-arguments that have shaped this discussion. We suggest that much of the controversy hinges on several misunderstandings, including unwarranted fears of a general attempt at overthrowing the Modern Synthesis paradigm, and some fundamental conceptual confusion about the proper roles of phenotypic plasticity and natural selection within evolutionary theory.
Key words: phenotypic plasticity, genetic assimilation, phenotypic accommodation, Modern Synthesis, natural selection, evolution
Introduction
Why revisit a 50 year old debate?
Genetic assimilation is a process whereby environmentally induced
phenotypic variation becomes constitutively produced (i.e. no longer requires
the environmental signal for expression). Although the origins of this concept
can be traced to the latter half of the 19th century
(Spalding, 1873
;
Baldwin, 1896;
Morgan, 1896;
Osborn, 1897), its formulation
in a genetic context was done independently in the 1940s by Waddington
(Waddington, 1942;
Waddington, 1952;
Waddington, 1953;
Waddington, 1961) and
Schmalhausen (Schmalhausen,
1949). All of these authors envisioned genetic assimilation as a
means of facilitating phenotypic evolution. By 1953, however, G. G. Simpson
had dismissed it: `... [genetic assimilation] is an interesting but, I
would judge, relatively minor outcome of the [synthetic] theory'
(Simpson, 1953), a sentiment
to be echoed by other writers, e.g. `It represents merely a degeneration
of a part of an original adaptation'
(Williams, 1966) and `a
baroque hypothesis' (Orr,
1999).
Despite such admonitions, interest in genetic assimilation continues to
increase, with a variety of updated conceptual treatments (e.g.
Rollo, 1994;
Schlichting and Pigliucci,
1998; Pigliucci and Murren,
2003; Price et al.,
2003; West-Eberhard,
2003; Schlichting,
2004; Badyaev,
2005). Recently, it has again been argued
(de Jong, 2005) that genetic
assimilation does not play an important role in evolution, and de Jong
asserted that the proposed updates are conceptually flawed. Here, we examine
her key criticisms:
To make sense of these arguments, and of why we consider that they miss the mark, we need first to briefly examine what phenotypic plasticity and genetic assimilation actually are. We will also need to briefly discuss the role(s) of quantitative genetics in evolutionary theory and practice, to address the charge that certain ideas about plasticity and assimilation are contradictory of established models in quantitative genetics.
Phenotypic plasticity and genetic assimilation: the basics
A fundamental issue about which there seems to be much disagreement
concerns the role(s) of phenotypic plasticity [concepts and methods have
recently been reviewed (Pigliucci,
2001)] and genetic assimilation (see below) within the context of
modern evolutionary theory.
|
).
Secondly, plasticity may be expressed at the behavioral, biochemical,
physiological or developmental levels; while all these phenomena share the
fundamental biological property of being part of the genotype-specific
repertoire of environmentally induced phenotypes, there are significant
differences in the degree of reversibility of different kinds of plasticity.
Typically, biochemical and physiological responses can be reversed over short
time scales, while developmental plasticity tends to be irreversible or takes
longer to be reversed. Thirdly, the type and degree of plasticity are specific to individual traits and environmental conditions; the same trait may be plastic in response to, say, changes in temperature, but not to nutrients, and a certain trait may be plastic in response to temperature while other traits are not. Finally, there seems to be abundant genetic variation for a variety of plastic responses in natural populations, which makes possible the evolution of plasticity by natural selection and other mechanisms.
As for genetic assimilation (GA), although it is Waddington's term that is
used, it is Schmalhausen's conception
(Schmalhausen, 1949) that is
closer to our modern interpretation. Waddington's experiments began by showing
that certain phenotypes [e.g. cross-veinless in Drosophila
melanogaster (Waddington,
1953)] can be obtained at low frequency in a population by an
environmental stimulus (e.g. heat shock at certain stages of development).
Today we would consider this a form of non-adaptive phenotypic plasticity
induced by stress. Waddington went on to select flies to increase the
frequency of the novel phenotype in response to the environmental stimulation.
In other words, he was selecting for that form of phenotypic plasticity to
become more frequent in the population
(Fig. 2). After relatively few
generations of selection he observed something unexpected: not only had the
frequency of the novel phenotype reached very high levels, but the
environmental stimulus no longer seemed necessary to elicit the appearance of
the cross-veinless phenotype! This apparent `inheritance of an acquired
character' was explained by Waddington in standard Darwinian terms as
selection on the activation threshold for the trait in question during
development. Waddington introduced the word `assimilation' to refer to this
outcome and discussed it in terms of canalization of the phenotype.
Schmalhausen's perspective (Schmalhausen,
1949) was similar to the modern view: his `stabilizing selection'
involved the exposure of hidden variation by a new environmental stimulus,
followed by selection for adaptive reactions to the stimulus, and finally
stabilization of the reaction norm.
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In summary, phenotypic plasticity is a common property of the reaction norm of a genotype (for a given trait, within a certain range of environmental conditions). Plasticity is what makes possible the appearance of an environmentally induced novel phenotype, and a process of selection on the expression of such phenotype in a new environment may end up `fixing' (genetically assimilating) it by altering the shape of the reaction norm.
Recent proposals about the roles of plasticity and assimilation
Before we can turn to an examination of the objections listed above, we need to have a better understanding of the substance against what exactly such objections have been raised.
Pigliucci and Murren make the claim that GA, long ignored as a phenomenon
of possible interest to evolutionary theorists despite Waddington's
experimental demonstration of its possibility, should be carefully
reconsidered (Pigliucci and Murren,
2003). They pointed to a significant amount of circumstantial
evidence that is compatible with partial or complete GA in several species of
plants and animals. In our view, phenotypic plasticity could facilitate the
expression of relatively well-adapted phenotypes under novel conditions (e.g.
after migration to a new geographical area), and therefore allow a population
to persist. Selection on the novel phenotype in the new environment would then
simultaneously alter the reaction norm [e.g. because of costs associated with
plasticity (Relyea, 2002;
van Kleunen and Fischer,
2005)], and improve the performance of the population, resulting
in the genetic assimilation of the trait in the new environment. This has the
potential to explain a variety of evolutionary ecological processes,
including, for example, the lag phase and successive population explosion of
many invasive species.
West-Eberhard's claims about the role of plasticity in evolution are more
sweeping (West-Eberhard,
2003), and result from a broad treatment of the general problem of
phenotypic evolution (see also Schlichting
and Pigliucci, 1998). West-Eberhard sees phenotypic evolution as
the result of four steps:
The scenario proposed by Pigliucci and Murren for GA via evolution
of plasticity (Pigliucci and Murren,
2003) would be a particular case of the broader possibility
envisioned by West-Eberhard, specifically when the origin of the trait (step
1) is due to an environmental, rather than a genetic, change. How prevalent
the situations proposed by these authors
(Pigliucci and Murren, 2003;
West-Eberhard, 2003) actually
are, is of course, a matter for empirical investigation.
Finally, several authors have pointed out that genetic assimilation may
also have broad evolutionary consequences through the integration of different
phenotypic characteristics (Pigliucci and Preston, 2004). Assimilation may
reveal, or even increase, the plasticity of traits correlated to the one being
assimilated because – by making the regulation of one trait (e.g. an
originally learnt behavior) independent of the presence of an environmental
stimulus – another trait (e.g. a correlated behavior) can be
conditionally expressed with much higher probability [the stretch-assimilate
principle (see Jablonka and Lamb,
2005)].
The critiques, and why they miss the mark
We are now in a better position to understand the criticisms of recent work on the potential role of plasticity and assimilation in evolution.
(1) `In genetic assimilation, phenotypic plasticity is not itself of
importance, but only an intermediate stage to a new genetically fixed and
phenotypically invariant state' [(de
Jong, 2005), p101]. de Jong claims that a focus on GA diminishes
the importance of phenotypic plasticity (PP) as an adaptive trait. We suggest
that she misses the point. In GA, plasticity is of paramount importance
because it allows the initial survival of the organism under novel
environmental conditions. However, if the new conditions are the only ones
being experienced by the population (i.e. the environment is not predictably
variable), then standard evolutionary theory predicts the loss of plasticity
and the evolution of a canalized phenotype: plasticity has led to
assimilation. On the other hand, when both the old and new environments
continue to be encountered, selection will favor the evolution of a reaction
norm that is appropriately plastic.
(2) `The adaptive role of phenotypic plasticity can be predicted from
[quantitative genetic] models, not as a consequence of a developmental
plasticity that is inherent to life and on a par with selection'
[(de Jong, 2005), p113]. Let us
deal with the second half of this statement first. To the best of our
knowledge, no one has ever suggested that plasticity plays a role in evolution
as a mechanism `on a par with' natural selection. Indeed, this would be what
philosophers of science refer to as a category mistake (as in asking `what is
the color of triangles?'), since plasticity is a mechanism in the sense of a
proximate cause of developmental (or biochemical, physiological, behavioral)
changes, while natural selection is an ultimate cause of adaptation during
evolution. Therefore, selection acts on developmental plasticity, and the two
simply cannot be considered alternatives from a logical standpoint.
Returning to the efficacy of quantitative genetic models, we need to
emphasize the distinction between two different roles of such models in
evolutionary biology (e.g. Pigliucci and
Schlichting, 1997). On one hand, quantitative genetics (QG) is a
body of theory aimed at developing simple mathematical models, such as those
presented by de Jong (de Jong,
2005), that can account in a general fashion for patterns of
phenotypic evolution in natural populations. In this sense, there is no doubt
that QG can `explain' the evolution of phenotypic plasticity. However, many
possible details of the specific mechanisms are equally compatible with any
particular model, so that the explanatory power is somewhat weakened, and
cannot reliably distinguish similar outcomes of different historical pathways
of evolution.
In the case of de Jong's QG model (de
Jong, 2005), her ability to claim that the evolution of ecotypes
requires no expression of hidden plasticity derives from the assumption that
trait values in different environmental states form a continuum. The result is
that trait's expression becomes `predictable' even in putatively novel
environments (but see Schlichting and
Pigliucci, 1998; Dudash et al.,
2005).
The problem worsens if one turns to the other aspect of QG, i.e. the
inference of possible causal mechanisms and/or historical paths, or the
prediction of future outcomes. Its statistical tool set aims at summarizing
the genetic variances and covariances among traits in a population, but while
it is true that any study of phenotypic diversity in natural populations has
to start with statistical summaries, it does not follow that such summaries
can profitably be used for inferential purposes. When de Jong, for example,
examines plots of reaction norms and their inter-environmental genetic
correlations, deducing the presence or absence of physiological mechanisms
underlying such patterns (de Jong,
2005), she is stepping far outside the reasonable boundaries for
such methods. As Shipley, for one, has convincingly argued
(Shipley, 2000), though
variance–covariance patterns can be used to generate testable causal
hypotheses, they most definitely cannot lead to trustworthy inferences about
underlying mechanisms. The reason for this is – again – the
well-known fact that many causal paths may lead to very similar phenotypic
outcomes, and the latter cannot be used to go back to the former, no matter
how clever and sophisticated the statistical tools. This is simply a fact of
life for biologists and quantitative scientists in general, and it will not do
to pretend otherwise.
Finally, with regard to the utility of QG models, we note that Price et al.
have modeled the evolution of peak shifts via genetic assimilation
using standard QG models (Price et al.,
2003). In their simulations, various levels of plasticity were
investigated: if plasticity was low, the population either went extinct or
remained `trapped' under the low peak; if plasticity was high, the peak shift
could be accomplished directly via plasticity and no genetic change
would be engendered. However, at intermediate levels of plasticity the
phenotype produced moves into the attractive domain of the higher peak, and a
period of constancy of this new environment leads to a peak shift via
genetic assimilation.
(3) `There is a good reason for that lack of attention [to genetic
assimilation as an evolutionary mechanism]: the lack of convincing
examples" [(de Jong,
2005), p. 16]. Similarly, genetic assimilation has been cavalierly
dismissed on the ground of lack of evidence: `unless and until there are
hard data demonstrating the frequent occurrence of assimilation, evolutionists
will rightly refuse to ground theories of adaptation on such a baroque
hypothesis' (Orr, 1999).
Pigliucci and Murren anticipated such criticism
(Pigliucci and Murren, 2003),
and warned that it makes little sense to deny the relevance of GA in evolution
on the basis of a current dearth of evidence. First, the process may require
only a few generations (as in Waddington's experiments), which means that it
could occur so rapidly as to pass below the radar screen of evolutionary
biologists, unless they were explicitly looking for it. Secondly, evolutionary
biology is a historical science
(Pigliucci, 2002), and in
historical research `evidence' is not simply out there for the taking, it
becomes an object of a search in light of specific hypotheses (we would do
well to remember Darwin's words in a letter to Henry Fawcett: `How odd it
is that anyone should not see that all observation must be for or against some
view if it is to be of any service!' Numerous cases, in diverse
organisms, have been identified that are compatible with the hypothesis of GA
(see Rollo, 1994;
Pigliucci and Murren, 2003;
West-Eberhard, 2003;
Tardieu, 1999; Chapman et al.,
2000; Cooley et al., 2001;
Sword, 2002;
Price et al., 2003;
Heil et al., 2004;
Mery and Kawecki, 2004;
Palmer, 2004;
Keogh et al., 2005), so it
seems that there is plenty of reasonable ground for advocating more explicit
tests of the possibility that GA occurs in natural populations.
Additionally, since Pigliucci and Murren
(Pigliucci and Murren, 2003)
and Schlichting (Schlichting,
2004), several theoretical approaches continue to examine genetic
assimilation under a variety of conditions (e.g.
Wiles et al., 2005). Recent
advances in the study of genetic assimilation include the use of computational
models (Downing, 2004), and
such models incorporate our current understanding of molecular biology
(Behera and Nanjundiah, 2004).
Other authors have taken a network modeling approach
(Masel, 2004), or used the
prisoner's dilemma framework (Suzuki and
Arita, 2004). Together, these studies demonstrate that genetic
assimilation is at least an active area of theoretical inquiry from a variety
of perspectives.
Moreover, we would argue that, if the onus of evidence is to be placed on supporters of GA, we might reasonably expect that its detractors likewise demonstrate evidence for their favored schema. For example, how many times has the evolution of ecotypes (e.g. as proposed in de Jong's models) been observed in nature or the laboratory? For critics of GA as a facilitator of speciation, how many times has speciation been observed without an initial phase of plasticity or phenotypic accommodation?
(4) `Phenotypic plasticity does not constitute a major alternative view
of evolutionary biology, but takes its legitimate place in the neo-Darwinian
modern synthesis' [(de Jong,
2005), p116]. de Jong's paper
(de Jong, 2005) can be seen as
an attempt to defend the Modern Synthesis [which she erroneously refers to as
the `neo-Darwinian' synthesis (Mayr and
Provine, 1980)] from a perceived attack by the likes of
West-Eberhard and the authors of the present paper. It is certainly true that
several authors have pointed out limitations of the current paradigm in
evolutionary biology, and have argued for inclusion of perspectives that have
been ignored or downplayed in the past. Examples are ideas about punctuated
equilibria, species selection, and the role of non-selective events in
macroevolution (Gould, 2002);
the elevation of environment to an equal role with genes
(Schlichting and Pigliucci,
1998; Lewontin,
2000); West-Eberhard's treatment of phenotypic accommodation
(West-Eberhard, 2003); and
most recently, Jablonka and Lamb's perspective on the importance of epigenetic
inheritance systems (Jablonka and Lamb,
2005).
All of these, however, have clearly been intended as extensions of the
Modern Synthesis, not rejections of it, just as the Synthesis itself has
always been interpreted (correctly) as an extension, not a rejection, of
Darwin's original insight that organismal history and diversification is
largely a result of common descent and natural selection
(Darwin, 1859). Indeed,
evolutionary biology may be one of the most glaring exceptions to philosopher
Thomas Kuhn's idea (Kuhn,
1970) that progress in science takes place through occasional
revolutions (paradigm shifts), as in the transition between the Ptolemaic and
the Copernican systems, or between the Newtonian and relativistic conceptions
of the universe. Since Darwin's original idea was, as far as we can tell,
essentially correct, it stands to reason that all the work of the Modern
Synthesis, as well as all current attempts to improve on the latter, are best
thought of as additional ramifications stemming out of the same base tree, not
as plots to uproot the Darwinian construction.
Concluding remarks
We think that the new ideas about phenotypic plasticity's role in evolution, as well as the re-evaluation of concepts such as GA and phenotypic accommodation, represent not a threat to the Modern Synthesis, but rather a welcome expansion of its current horizon. Moreover, these ideas are generally compatible with current quantitative genetic models of phenotypic evolution (because the latter are largely invariant with respect to specific mechanisms), and offer the potential for a fruitful empirical research program that need not be prematurely quashed due to superficial critiques.
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), and we think
the reason for this is some persistent level of conceptual confusion about the
proper domains of terms such as natural selection, phenotypic plasticity, and
genetic assimilation. Fig. 3
shows how these are actually related: phenotypic plasticity is (in part) a
developmental process, not an evolutionary one. As such, it can be the target
of natural selection (an evolutionary mechanism, though of course not the only
one), and yield – under certain conditions – the evolutionary
outcome of genetic assimilation or phenotypic accommodation. Once one
recognizes the clear hierarchical distinctions among these concepts, most
fears about an imminent overthrow of the Modern Synthesis should
dissipate. Acknowledgments
We thank James Fordyce, Theodore Garland and Trevor Price for their helpful feedback, and Josh Banta for reading a previous draft of the manuscript.
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