Evolution as Frozen Music

Les Schaffer schaffer at optonline.net
Fri Aug 8 12:20:02 MDT 2003

Evolution as Frozen Music
A review by Jeffrey S. Levinton*

Developmental Plasticity and Evolution 
by Mary Jane West-Eberhard
Oxford University Press, New York, 2003. 814 pp. $100, £79.50. 
ISBN 0-19-512234-8. Paper, $49.95, £31.99. ISBN 0-19-512235-6.


Johann Wolfgang von Goethe, the great poet, amateur musician, and
biologist, saw architecture as "frozen music." His metaphor can be
extended to the development of organisms under the influence of the
previous history of the evolutionary process. As I listened the other
night to Van Cliburn playing a piano concerto, I heard Beethoven's
score transformed into a highly structured phenotype of sound. The
music was influenced by the pianist's forceful hand; by the localized
and organized sounds that flowed from the conductor's motions to the
double bases one moment, to the violins another; and perhaps even by
the windy evening's gusts and the patter of raindrops. The biological
phenotype is no less shaped by its DNA score, though we have much to
learn about the role of the environment in shaping its development and
about how a variety of developmental branching points can lead to
different outcomes of frozen music. Evolutionary biologists have, in
the service of theoretical convenience, visualized a population of
heritable scores from which some are selected--by differential
mortality and reproductive success, which lead to increased
fitness--to play the best tune; their focus has generally been on how
genes and traits propagate or are lost. In Developmental Plasticity
and Evolution, Mary Jane West-Eberhard addresses the crucial question
of how novel forms arise.  West-Eberhard, an evolutionary biologist at
the Smithsonian Tropical Research Institute, is a specialist in the
natural history, behavior, and evolution of social wasps. Inspired by
the perception of a "failure of evolutionary biology to deal
effectively with complex adaptive plasticity," she offers a new
synthesis of development and evolution. Her complete theory
incorporates the effects of the environment on plastic phenotypic
responses, the ontogeny of organized alternative phenotypes turned on
by developmental switches, the mechanisms by which environmental
influences initially maintain these phenotypes and then increase their
frequencies, and, finally, the evolutionary incorporation of these
frequency shifts.

West-Eberhard bases her theory on three major precepts. First, because
of phenotypic plasticity and the common amplification of environmental
effects by behavioral responses, environmental induction often
initiates adaptive evolutionary change. For example, she cites
well-known effects of changes in food concentration on the form of
skeletons and ciliary bands of larval sea urchins. She also
resuscitates James M. Baldwin's theory, which argues that the behavior
of appropriately responding individuals can accelerate their exposure
to new environments, exposure that (if they are genetically distinct)
enhances their role as players in evolutionary change.

Second, the organized nature of development produces, through
phenotypic plasticity, quantally distinct new
phenotypes. West-Eberhard considers genes to be followers, not
leaders, in evolutionary change. She sees developmental switches as a
source of evolutionary creativity. Instead of constraining change,
they produce distinct alternative phenotypes, whose deleterious
pleiotropic effects are fewer than previously thought. Negative
pleiotropy can be further reduced by "character release." Owing to an
environmental shift, the new, plasticity-induced phenotype becomes
dominant in the population, and subsequent evolutionary rearrangement
of genetic modifiers then increases its independence from other
aspects of the phenotype. The theory depends on a notion of "extreme
modularity," which "leads to extreme developmental independence of the
parts, and, consequently, to a capacity for extreme specialization of
traits." Switches are the plasticity-induced focal point for
evolutionary change. Because plasticity can induce the new phenotypes,
the problem of the loss of rare mutants due to stochastic factors is
greatly reduced and the probability that the change will spread in a
population is increased. The storehouse of developmental potential is
always at the ready. The induction of alternative phenotypes may be
predictable, which could lead to recurrent appearances of a trait
throughout the history of a clade. The theory is not Lamarckian,
because the induced phenotypes must have some genetic distinctiveness
in order to be recruited into the evolutionary process.

Third, phenotypic plasticity can facilitate evolution by
accommodating, and even exaggerating, changes in the production of new
phenotypes. Shifts in the environment, for example, can result in the
dominance of a phenotype that was formerly present, though in lower
frequency. Thus, the traditional standing genetic polymorphism that
figures so prominently in most population-level models of evolution is
seen as secondary in importance (though not absent). Nevertheless, the
model is quintessentially one that operates at the population
level. Although speciation may separate a new evolving line, the
evolutionary transition does not require speciation for
change. Indeed, West-Eberhard posits a continuity in the evolutionary
process from below the level of species to above it.

West-Eberhard is arguing for a development-centered approach to the
investigation of phenotypic variation. As she notes, "The causal chain
of adaptive evolution...begins with development." This claim is
exactly on the mark, but it seems to me that evolutionary biologists
have, to a large extent, already abandoned the notion that mutations
are always random and have accepted development as the correct
framework for the search for mutants and population-level evolutionary
change. Therefore, this part of the author's argument crashes through
an open door, even if that door has only recently been opened wide by
evolutionary developmental biologists and geneticists.

What will be regarded as novel is West-Eberhard's belief that
environment- induced variation, guided by the predictability of
development that produces alternative phenotypes, is the major stuff
of evolution. One exciting outcome of this theory is the possibility
of investigating major evolutionary change at the population
level. (However, some changes may have been lost in the early history
of organisms when some fundamental new phenotypes--such as the
arthropod exoskeleton--were incorporated.) West-Eberhard bolsters her
argument with many examples that suggest how environmental effects on
phenotypic plasticity might cause organized, quantum leaps in
evolutionary change and how (owing to the organized nature of
development) these leaps might predictably recur in a phylogenetic
history. Yet many of these examples are little more than well reasoned
and mildly convincing conjecture, and many are also open to
interpretation by means of the more traditional,
mutation-followed-by-selection arguments.

Those skeptical of West-Eberhard's theory will ask for answers to a
number of crucial questions and tests. Most important, known
phenotypic plasticity will have to be examined carefully. Is such
plasticity generally a source of evolutionary creativity? Or is it
normally only a product of previous gradual adaptive evolution? Do
behavioral responses usually follow Baldwin's theory? Or is behavior
more frequently a buffering factor, one that acts largely as a
centripetal force in evolution? Especially needed is an algebraic
formulation that will allow researchers to evaluate the frequency of
plasticity and behavioral accommodation to environmental change, the
phenotypic costs of developmental variation, and the competition
between these processes and genetically based variation.

Also necessary is an unbiased consideration as to whether organized
developmental alternative phenotypes actually appear so frequently and
predictably without strong negative pleiotropies. The multiple paths
known to operate in similar evolutionary changes (for example, in
neoteny of salamanders) suggest that organized phenotypes may be ad
hoc affairs and not inevitable alternative outcomes of
development. Are developmental switches so readily available to
generate novel phenotypes? Or did they evolve to turn on particular
developmental processes with occasional and unpredictably strong
negative consequences when altered? After all, in sea squirts the manx
gene appears to cause the loss of the tail and other characters
involved in phylum-level change (1); whereas in cats the Manx locus
dominant M allele reduces tail length as a heterozygote (Mm), but
leads to death in utero when homozygous (MM). The character of
pleiotropy is clearly not predictable at present.

In addition, researchers will have to determine whether genetic
organization can be ignored so readily as West-Eberhard manages to
do. The example of Hox genes argues that we must be careful in
ignoring gene arrangement, and the dominant role of gene regulation in
morphology is a story that has yet to be told completely (2). Will
developmental phenotypes typically involve a set of interactive
enhancers that are tissue-specific and genetically localized? Only
careful genetic analysis will be able to answer such questions.

Despite these many challenges to West-Eberhard's provocative
explanations, Developmental Plasticity and Evolution is a forceful
volume. Filled with an impressive repetoire of examples and strong
imaginative lyrics, it demands a careful examination with an open


B. J. Swalla, W. R. Jeffery, Science 274, 1205 (1996). 
M. Levine, R. Tjian, Nature 424, 127 (2003). 

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