Natural Selection and Canalization and Assimilation
From: Michael Ragland (ragland37_at_webtv.net)
Date: 09/23/04
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Date: Thu, 23 Sep 2004 17:50:38 +0000 (UTC)
"The primary phenotype, which RENDEL calls Make, is the total amount of
this substance that would be produced in the absence of regulation,
while the expressed phenotype is proportional to the amount of substance
that actually becomes available as a result of the interaction of the
primary determinants with the regulatory system. The contributions to
Make of major genes, minor genes and environment are additive. The
regulatory system functions as a repressor of the major genes. As long
as the level of Make is not larger than the amount, M0, required to
obtain the desired expression of the trait, repression is silent and the
resulting trait is proportional to Make. When, instead, the level of
Make begins exceeding M0, repression of the major genes is activated so
as to keep the actual production of morphogenic substance as close as
possible to M0. Since regulation only operates on the major genes, this
production cannot be depressed below that part of Make that is caused by
minor genes and environment. In addition, a certain portion of the
contribution of major genes might also be nonregulatable. Thus, if the
part of Make that cannot be regulated is itself larger than M0, the
expression of the trait will exceed the desired level and will increase
as Make increases. It is therefore clear that regulation is effective
only as long as Make is contained within the canalization range R = [M0,
M0 + m], where m denotes the regulatable portion of major genes'
contribution to Make. If the major genes are selected for optimal
production, as in the wild type, Make usually falls in the canalization
range and all moderate variations because of minor genes and environment
are damped out.
If the wild-type alleles of a major locus are replaced by mutations, or
major external disturbances intervene, Make may go out of range and
underlying variation is exposed.
Since canalization promotes the accumulation and preservation of a large
store of hidden genetic variation, which could be exposed and rapidly
exploited by natural selection in case of sufficiently drastic
environmental changes, RENDEL 1967 (pp. 148–157) considered that it
must have important effects on the mode and rate of evolution. In fact,
he argued that in the course of evolution long phases of phenotypic
stasis, during which canalization systems are redirected and refined,
should alternate with rapid shifts when the phenotype migrates to a new
adaptive peak, a view that anticipates the more recent theory of
punctuated equilibria "
http://www.genetics.org/cgi/content/full/149/4/2119
Genetics, Vol. 149, 2119-2133, August 1998, Copyright © 1998
Canalization, Genetic Assimilation and Preadaptation: A Quantitative
Genetic Model
Ilan Eshela and Carlo Matessib
a Department of Statistics, School of Mathematics, Tel Aviv University,
69978 Tel Aviv, Israel
b Istituto di Genetica Biochimica ed Evoluzionistica, Consiglio
Nazionale delle Ricerche, 27100 Pavia, Italy
Corresponding author: Carlo Matessi, Istituto di Genetica Biochimica ed
Evoluzionistica, Consiglio Nazionale delle Ricerche, Via Abbiategrasso
207, 27100 Pavia, Italy., matessi@ipvgbe.igbe.pv.cnr.it (E-mail).
Communicating editor: M. K. UYENOYAMA
ABSTRACT
MORPHOGENIC AND SELECTING...
ADAPTIVE INACTIVATION OF THE...
COEVOLUTION OF THE CANALIZING...
DIRECTED PREADAPTATION,...
SOME SUGGESTIONS FOR THE...
DISCUSSION
LITERATURE CITED
We propose a mathematical model to analyze the evolution of canalization
for a trait under stabilizing selection, where each individual in the
population is randomly exposed to different environmental conditions,
independently of its genotype. Without canalization, our trait (primary
phenotype) is affected by both genetic variation and environmental
perturbations (morphogenic environment). Selection of the trait depends
on individually varying environmental conditions (selecting
environment). Assuming no plasticity initially, morphogenic effects are
not correlated with the direction of selection in individual
environments.
Under quite plausible assumptions we show that natural selection favors
a system of canalization that tends to repress deviations from the
phenotype that is optimal in the most common selecting environment.
However, many experimental results, dating back to WADDINGTON and
others, indicate that natural canalization systems may fail under
extreme environments. While this can be explained as an impossibility of
the system to cope with extreme morphogenic pressure, we show that a
canalization system that tends to be inactivated in extreme environments
is even more advantageous than rigid canalization.
Moreover, once this adaptive canalization is established, the resulting
evolution of primary phenotype enables substantial preadaptation to
permanent environmental changes resembling extreme niches of the
previous environment.
THE concept of genetic assimilation was introduced by WADDINGTON 1953 ,
WADDINGTON 1961 to highlight the remarkable outcome of several
artificial selection experiments in which an environmentally induced
phenotypic modification became expressed even in the absence of the
external stimulus that was initially necessary to induce it. For
example, when pupae from a laboratory population of wild-type Drosophila
melanogaster were exposed to heat shock, some of the emerging adults
exhibited a gap in the posterior crossveins of the wings that is not
normally observed in untreated flies (WADDINGTON 1952 , WADDINGTON 1953
After some generations of selection, when only these abnormal
individuals were allowed to breed, the proportion of adults with broken
crossveins induced by heat shock at the pupal stage was raised above 90%
and, moreover, a small proportion of individuals were crossveinless even
among flies that had not been exposed to temperature treatment. If
artificial selection was then continued by breeding the adults that had
developed the abnormality without heat shock, the frequency of
crossveinless individuals among untreated flies became very high,
reaching 100% in some lines. Genetic assimilation has been repeatedly
demonstrated in Drosophila for a variety of morphological traits and
environmental stresses (e.g., WADDINGTON 1956 ; BATEMAN 1959A , BATEMAN
1959B ).
As explained by WADDINGTON, the development of crossveins and other
apparently very stable morphological traits can be influenced by
environmental disturbances above a certain threshold of intensity, but
individuals from wild-type populations have a threshold so high that
only an unusually strong stimulus, such as a heat shock, can effectively
induce a modified expression. According to WADDINGTON's explanation, the
phenotypic uniformity generally observed in these traits can easily
coexist with the abundant genetic variability demonstrated by artificial
selection in assimilation experiments. Although different genotypes
available in a population are sensitive to different threshold values of
external stimuli, phenotypic variation does not arise if all of them
have too high a threshold to be affected by the disturbances prevailing
in the usual environment. However, when an exceptionally severe
disturbance occurs, the subpopulation of individuals in which a
phenotypic change is induced is necessarily enriched for the most
sensitive genotypes, which provide the material for artificial
selection.
The peculiar pattern of interaction between genetic and environmental
variation that underlies the expression of crossveins, and of other
traits that can be similarly subject to assimilation, was described by
WADDINGTON using the concept of genetic canalization (WADDINGTON 1940 ).
When the expression of a trait is well canalized, most genetic and
environmental variation has no, or very little effect on the phenotype,
so that a population remains phenotypically uniform even if it contains
substantial genetic heterogeneity, or is exposed to wide fluctuations of
the environment. For this reason, it is expected that canalization is
tighter for those traits that most crucially contribute to fitness
(WADDINGTON 1941 ; SCHMALHAUSEN 1949 ). Phenotypic effects, however, can
be produced if individuals are subject to severe perturbations and, in
this respect, genetic and environmental factors are considered largely
equivalent from the point of view of canalization (WADDINGTON 1961 ).
Thus a mutation at a major locus and an external shock can produce
identical changes on a trait, as demonstrated by phenocopies. The
distinctive aspect of canalization, which makes assimilation possible
(WADDINGTON 1942 , WADDINGTON 1961 ), is the fact that, once the
expression of a trait is modified by a sufficiently severe perturbation,
the effects of minor factors that are normally repressed also become
exposed, resulting in a substantial increase of phenotypic variation in
the population.
The nature and the genetic bases of canalization have been studied in
detail by RENDEL and by several other authors (RENDEL 1959 ; RENDEL and
SHELDON 1960 ; also, e.g., DUN and FRASER 1958 , DUN and FRASER 1959 ;
MILKMAN 1960 , MILKMAN 1961 ). A thorough review and careful
interpretation of the results was given by RENDEL 1967 . Instead of an
environmental stress as a tool to uncover hidden variation for bristle
number in the scutellum of D. melanogaster, RENDEL used a recessive
mutant allele, sc1, of the sex-linked locus scute.
In flies of the wild type the number of bristles is essentially fixed at
four, variant individuals being exceedingly rare. In unselected mutant
stocks, however, the average number of bristles is about 1.0 for females
(sc1/sc1) and 0.5 for males (sc1) and variability is quite high as, for
example, only 33% of females have one bristle. Most of this increased
variability, however, is not intrinsic to the mutant allele. In fact,
after a population in which sc1 and the wild-type allele (+) were
segregating was subject to selection for a high number of bristles, the
sc1/sc1 genotype reached a mean of almost four bristles and variation
was substantially decreased (e.g., only 12% of individuals differed from
the mean), while in the +/+ genotype, where the mean had become about
eight, variation was increased dramatically (ranging from four to twelve
bristles). Clearly, in these populations development of scutellar
bristles is subject to powerful canalization to prevent variation around
four bristles and it is only when it is forced to deviate far from this
target that underlying variation is expressed. Moreover, the target of
canalization on the phenotypic scale is under genetic control and can be
displaced by selection. This was demonstrated by RENDEL and SHELDON 1960
who, by artificial selection for low variability in a population
homozygous for sc1, were successful in shifting the canalization to
around two bristles. Canalization of the unstable expression of mutant
traits was also obtained in several other artificial selection
experiments in Drosophila (MAYNARD SMITH and SONDHI 1960 ; WADDINGTON
1960 ) and in the house mouse (KINDRED 1967 ).
These and several other results obtained by different authors can be
nicely explained by a model proposed by RENDEL 1967 to describe a simple
system of regulation leading to canalization. According to this model, a
canalized trait is determined by four kinds of factors: (i) one or a few
major genes, (ii) a number of minor genes, (iii) environmental factors
and (iv) the regulatory system. Both major and minor genes, subject to
environmental effects, are responsible for the production of a
morphogenic substance of some kind. The primary phenotype, which RENDEL
calls Make, is the total amount of this substance that would be produced
in the absence of regulation, while the expressed phenotype is
proportional to the amount of substance that actually becomes available
as a result of the interaction of the primary determinants with the
regulatory system. The contributions to Make of major genes, minor genes
and environment are additive. The regulatory system functions as a
repressor of the major genes. As long as the level of Make is not larger
than the amount, M0, required to obtain the desired expression of the
trait, repression is silent and the resulting trait is proportional to
Make. When, instead, the level of Make begins exceeding M0, repression
of the major genes is activated so as to keep the actual production of
morphogenic substance as close as possible to M0. Since regulation only
operates on the major genes, this production cannot be depressed below
that part of Make that is caused by minor genes and environment. In
addition, a certain portion of the contribution of major genes might
also be nonregulatable. Thus, if the part of Make that cannot be
regulated is itself larger than M0, the expression of the trait will
exceed the desired level and will increase as Make increases. It is
therefore clear that regulation is effective only as long as Make is
contained within the canalization range R = [M0, M0 + m], where m
denotes the regulatable portion of major genes' contribution to Make. If
the major genes are selected for optimal production, as in the wild
type, Make usually falls in the canalization range and all moderate
variations because of minor genes and environment are damped out.
If the wild-type alleles of a major locus are replaced by mutations, or
major external disturbances intervene, Make may go out of range and
underlying variation is exposed.
Since canalization promotes the accumulation and preservation of a large
store of hidden genetic variation, which could be exposed and rapidly
exploited by natural selection in case of sufficiently drastic
environmental changes, RENDEL 1967 (pp. 148–157) considered that it
must have important effects on the mode and rate of evolution. In fact,
he argued that in the course of evolution long phases of phenotypic
stasis, during which canalization systems are redirected and refined,
should alternate with rapid shifts when the phenotype migrates to a new
adaptive peak, a view that anticipates the more recent theory of
punctuated equilibria (ELDREDGE 1971 ; ELDREDGE and GOULD 1972 ).
Basically the same mode of evolution was predicted by SCHMALHAUSEN 1949
in his theory of stabilizing selection, which introduced genetic
concepts closely related to canalization, and by WADDINGTON 1957 ,
WADDINGTON 1961 who, in particular, maintained that genetic assimilation
plays an important evolutionary role by generating substantial
phenotypic innovations and accelerating adaptation to foreign
environments. In fact, according to his view, as soon as a population
faces a sudden but lasting alteration of the environment, or colonizes
an unfamiliar habitat, a number of phenotypic changes are likely to
emerge, directly induced by stressful external conditions. Some of these
changes, being more suitable to the present environment than the current
wild type, will help the population to survive through the critical
situation and at the same time will provide natural selection with
genetic variation that the process of assimilation can rapidly use to
stabilize and improve the new adaptation.
WADDINGTON's theory has been refuted by WILLIAMS 1966 who, without
denying the reality of genetic assimilation, argued strongly against the
significance of its role in the process of adaptation. Missing
crossveins and other anatomical anomalies utilized in assimilation
experiments reflect disruptions of development caused by exceptionally
severe external perturbations. It is only through the artificial
selection imposed by the experimental design that assimilation of these
characters can be successful in the laboratory. As maintained by
WILLIAMS, phenotypic modifications of this kind, which are a direct
result of environmental interferences to which the species is not
prepared to respond, are likely to be disadaptive under most
circumstances and, even if there were a condition in which any of these
would be adaptive, we should expect it to be quite different from the
condition that is specifically required to induce the given variation
directly. Thus, if certain extreme situations become recurrent or
permanent, any phenotypic change that they could cause would be
eliminated by natural selection rather than assimilated. Phenotypic
disruptions directly induced by the environment are, therefore, not
expected to provide useful material for any evolutionary progress.
WILLIAMS also discussed the role of assimilation in relation to a very
different form of phenotype-environment interaction, which generally is
referred to as (adaptive) plasticity. This occurs in the many cases in
which an organism is able to respond to changing conditions of the
environment with specific modifications of certain traits, in a way that
is appropriate to preserve the quality of its vital activities. This
kind of phenotypic reaction to external stimuli is obviously a
sophisticated adaptation to variability of the environment, which can
only be achieved through a complex and slow process of natural selection
(VIA and LANDE 1985 ; DE JONG 1990 , DE JONG 1995 ; SCHEINER and LYMAN
1991 ; GOMULKIEWICZ and KIRKPATRICK 1992 ; GAVRILETS and SCHEINER 1993 ;
ZHIVOTOVSKY et al. 1996 ). Once a trait has evolved plasticity in this
way, it could become a target of genetic assimilation whenever some
appropriate varying factor of the environment becomes more stable. In
fact, in the new situation, there is a selective advantage for the
genotypes that more reliably express the particular state of the trait
that is most adequate to the level of the external factor that now
prevails.
Assimilation in a plastic trait of D. melanogaster has been demonstrated
by WADDINGTON 1959 and, more recently, by TE VELDE et al. 1988 in
experiments concerning the morphology of anal papillae, a larval organ
that is involved in the regulation of osmotic pressure of internal
fluids. When larvae are reared in a medium with salinity sufficiently
high to cause substantial mortality, their anal papillae become,
relative to body size, slightly larger than those of larvae grown in
normal media.
The macroscopic change of these organs is associated with adaptive
modifications in the ultrastructure of their membranes (TE VELDE et al.
1988 ), which apparently function in the regulation of ion exchange. In
WADDINGTON's experiments, a number of populations were maintained under
conditions of high salt concentration for several generations. No
artificial selection was applied, so that the populations were subject
only to natural selection, driven mainly by the larval mortality caused
by the elevated salinity of the medium.
As a result, at the end of the experiments the selected strains were
better adapted to high salt concentrations, since larval mortality had
decreased in comparison to the initial populations. In addition,
significant genetic assimilation had occurred because larvae from the
selected strains retained enlarged anal papillae even when reared in a
medium of normal salinity.
Thus, just as WILLIAMS pointed out, when genetic assimilation is applied
to a plastic trait, the result is the loss of a flexible response, which
is replaced by a stereotyped expression of the trait, a condition that
in many respects can be regarded as a more elementary mode of
adaptation. Hence, from his analysis WILLIAMS could conclude that
genetic assimilation is not, as WADDINGTON maintained, a major factor in
the emergence of new adaptations, and, when it plays a role in evolution
it has, in fact, the contrary effect of simplifying and restricting the
range of response of plastic traits.
Canalization is a widely recognized and well-documented phenomenon that
continues to be a topic of lively research. STEARNS and KAWECKI 1994 ,
analyzing the extent of canalization of various life-history traits in
D. melanogaster, have found that, as predicted by WADDINGTON,
canalization is more effective for traits to which fitness is more
sensitive. The same kind of data have been used by STEARNS et al. 1995
to demonstrate that the patterns of canalization against genetic and
environmental disturbances are closely parallel, suggesting that a
single regulatory mechanism keeps in check both sources of variation, in
agreement with RENDEL's model.
On the theoretical side, GAVRILETS and HASTINGS 1994 have proposed a
quantitative-genetic model of canalization against environmental
disturbances in a trait subject to selection. They show that when
selection on the trait is stabilizing, tighter canalization readily
evolves in a way that could preserve, or even increase, the heritability
of the trait, a feature that has been observed in experiments with
artificial stabilizing selection. The model of WAGNER et al. 1997 also
analyzes evolution of canalization, but takes into account both
environmental and genetic perturbations. These recent studies are just
the latest issues in a long tradition of mathematical research on
selection for the regulation of phenotypic variability. Particularly
interesting in this broader context are the results of LEVINS 1965 and
of SLATKIN and LANDE 1976 , concerning a quantitative trait subject to
optimizing selection in a fluctuating environment, such that the optimal
phenotype varies form one generation to the other. Though these two
works differ in their modeling approach and in the quantitative details
of the results, they basically agree in the main prediction that, if
fluctuations of the environment are moderate enough, selection would
favor any repression of phenotypic variation (e.g., through
canalization), but, if the environment fluctuates widely, selection
favors instead genetic systems that preserve or, maybe, amplify the
expression of phenotypic variations. In the recent literature there is a
growing interest in fluctuating asymmetry, namely the occurrence of
random differences between left and right in traits that normally have
bilateral symmetry. In the past, there has been disagreement as to
whether variability of this type truly indicates poor canalization
(e.g., MATHER 1953 ; REEVE 1960 ; WADDINGTON 1961 ; KINDRED 1967 ;
RENDEL 1967 , pp. 134–135), but now this property is widely used as a
tool to evaluate, even at the individual level, the quality of
canalizing systems, and the extent of genetic and environmental stresses
on development (MACKAY 1980 ; MAYNARD SMITH et al. 1985 ; PARSONS 1992
). A variety of estimation procedures and criteria to distinguish it
from other forms of asymmetry has been developed (PALMER and STROBECK
1986 ). CLARKE and MCKENZIE 1987 used fluctuating asymmetry to evaluate
the impact on developmental stability of insecticide resistance genes,
which spread in wild populations of the Australian sheep blowfly,
Lucilia cuprina, after introduction of insecticides. They found that
newly established resistance alleles induce an increase of fluctuating
asymmetry in bristle counts and other traits. However, if an allele has
been maintained in a population for a sufficiently long time by the
continued use of the insecticide that selected for resistance, levels of
fluctuating asymmetry are as low as in flies of the susceptible strains.
These effects are not intrinsic to specific resistance alleles but are a
property of the genetic background. In fact, if a resistance allele from
a wild strain with low asymmetry is transferred to the extraneous
genetic background of a susceptible strain, asymmetry increases again.
These results confirm the notion that variation of well canalized traits
can be exposed by major genetic perturbations of any kind and,
supplementing older results on artificial selection, provide evidence
that canalization systems are modified by natural selection.
Arguing from the experimental evidence that in several cases females
have a preference for males with symmetrical ornaments, some authors
(MOLLER 1992 ; MOLLER and POMIANKOWSKI 1993 ) have proposed the
hypothesis that females may use fluctuating asymmetry or, in general,
the degree of regularity of elaborate secondary sexual characters, as a
reliable cue to the genetic quality of their potential mates. Thus,
according to this hypothesis, canalization might be the actual target of
female preference and the basis of sexual selection.
Given that canalization is a rather general property of adaptive traits,
it is important to consider again the theoretical question of whether
the large unexpressed store of genetic variation that it can preserve
could play a significant role in the evolution of new adaptations. To be
valid, a positive answer should overcome the flaw that WILLIAMS found in
WADDINGTON's assimilation hypothesis. In this article we develop a
quantitative model to analyze the evolution of canalization of a
genetically determined trait subject to stabilizing natural selection.
When not canalized, expression of the trait is affected by random
environmental perturbations. Variability of the environment also
influences the pattern of selection, in that in each particular
environment, to which an individual is randomly assigned, a different
trait-value would be optimal. Taking into account the reservations of
WILLIAMS, we assume that the morphogenic influence of a deviation of the
environment from normal does not necessarily lead to a phenotype that is
better adapted to this specific deviation. We take into consideration,
though, the possibility that activation or inactivation of the
canalization system itself, like any other physiological feature, might
be affected by some general environmental factor such as stress,
irrespective of the selective advantage or disadvantage of the resulting
phenotype. If so, it is natural to further assume that the way the
environment affects the canalization system is controlled by genes, that
these genes are subject to variations and that such genetic variations
are also subject to natural selection.
In the framework of this structure we find that, under the same
conditions that enable the evolution of a rigid canalization system as
envisaged and studied by RENDEL, a more flexible, so to say adaptive
system of canalization is always advantageous for the individual
organism. We show next that the very development of such an adaptive
canalization system elicits, in turn, further evolution of the selected
trait. This evolution is such that, in the long term, the population
acquires a substantial degree of preadaptation to possible sudden,
permanent changes of the environment that resemble some rare
environmental condition of old. These processes may account for
long-term evolutionary modes such as punctuated evolution and, possibly,
atavism. As it turns out, though, short-term testable predictions of the
suggested adaptive canalization model are, in most though not in all
aspects, very much similar to predictions drawn from the model of
RENDEL. While both models seem to fit equally well the bulk of
experimental results of WADDINGTON and others, we attempt to point out
some crucial differences between the two sets of predictions, and, thus,
some possible experimental designs that may tell one from the other.
"It's uncertain whether intelligence has any long term survival value.
Bacteria do quite well without it."
Stephen Hawking
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