Toward a Postmodern Synthesis

Molds, Molecules, and Metazoa: Growing Points in Evolutionary Biology by Peter R. Grant;
Henry S. Horn
Review by: Rick Grosberg
Ecology, Vol. 74, No. 5 (Jul., 1993), pp. 1603-1605
Published by: Ecological Society of America
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REVIEWS

Ecology, 74(5), 1993, pp. 1603-1605

C) 1993 by the Ecological Society of America

TOWARD A POSTMODERN SYNTHESIS

Grant, Peter R., and Henry S. Horn (eds.). 1992. Molds,

molecules, and metazoa: growing points in evolutionary biology. Princeton University Press, Princeton. x + 181 p. $32.50,
ISBN: 0-691-08768-7.

One of the most influential books in my own ontogeny as

an evolutionist and ecologist was John Tyler Bonner's Size
and cycle. In this book, and many to follow, Bonner eloquently
reiterated and elaborated Walter Garstang's view that natural
selection acts on traits embedded in temporally dynamic life
cycles, rather than on static traits lifted out of their developmental context. As such, life cycles become the target of
natural selection, and thus the interests of both evolutionary
and developmental biology converge from the top down and
the bottom up at the level of the life cycle. Bonner continues
to explore both the conceptual and empirical dimensions of
this view toward evolution and embryology, and in so doing,
remains among the most persistent, sane, and lucid advocates
for building a new synthesis between developmental and evolutionary biology.

Molds, molecules, and metazoa. growingpoints in evolutionary biology contains a series of essays derived from a
symposium to celebrate the career of John Bonner. The editors of the collection of essays claim that, "the theme of the
symposium was simply evolution," and that the six authors
"were invited to contribute to the symposium by charting the
future course at six major growing points in the study of
evolution." This is a rather bold invitation, and the fact of
the matter is that most of the authors appropriately limit their
analyses to the two intriguing questions that Bonner poses in
the opening chapter: "why does one have development at all,
and since one does, how is it affected by evolution?" All six
remaining papers in the symposium address these questions
on levels of resolution ranging from geological to physiological
time, and from paleontological, behavioral, ecological, morphological, and molecular perspectives.
The first of the six "prospective" chapters, by James Valentine, chronicles the explosive history of early metazoan
diversification, and then considers two facets of the pattern
of diversification. First, Valentine seeks to understand why
so many body plans evolved, and evolved so rapidly, during
the earliest annals of the Metazoa. He offers the deceptively
simple answer that by the late Vendian/early Cambrian, enough
different types of cells had evolved so that they could collaborate to form histologically and functionally complex tissues
and organs. This, in turn, promoted the diversification of body
plans. The second issue concerns the identification of diagnostic attributes of major taxa that could explain macroevolutionary patterns of persistence and failure. In principle, this
amounts to an argument against Stephen Jay Gould's view
that the history of life is largely a lesson in historical stochasticity (see, for example, Gould's (1989) book Wonderful
life. W. W. Norton, New York). Like Valentine, I find such
interpretations frustrating because they are often explicitly or

implicitly antimechanistic, and because they tend to dismiss,

or trivialize, contrary data by implying that the findings are
not general (e.g., N. J. Butterfield. 1990. A reassessment of
the enigmatic Burgess Shale fossil Wiwaxia corrugate (Matthew) and its relationship to the polychaete Canadia spinosa
Walcott. Paleobiology 16:287-303). On the other hand, without an elaboration of why they resist extinction, Valentine's
conclusion that the taxa which come to dominate the biosphere are those which resist extinction is not substantially
more mechanistic. Valentine's essay takes us to the brink of
the perversely inviting chasm that separates microevolutionary processes from macroevolutionary pattern; but I still await
a clear view down, or a safe route across.
Graham Bell's essay starts with the lament that there is no
quantitative theory of the environment that rivals the theoretical foundation of population genetics. In response, Bell
sets out to elaborate a set of five "properties" of the environment which would presumably be the governing principles
for an ecological framework that predicts how organisms should
evolve. All of these properties are inferred from a limited
number of well-controlled, exceptionally detailed field and
laboratory studies on crop plants, forest herbs, and algae. The
first property is that the contribution of the environment to
phenotypic variance is far greater than the contribution of
genotype. The second property is an important corollary of
the first: environmental variance increases at all spatial scales
(and perhaps temporal scales), although the magnitude of the
variance will likely be smaller over smaller spatial scales and
shorter temporal scales. The third property moves into the
realm of relationships between organisms and their environments. In short, it states that genotype by environment interactions are so pervasive that norms of reaction of different
genotypes often cross; consequently, fitness rankings of particular genotypes should often change across selective regimes.
The fourth property acknowledges that environments themselves can evolve, not only from "forcing by external physical
factors," but also because organisms modify their physical
and biotic environments. The fifth property elaborates and
extends the fourth: through competitive and (more importantly, in his view) antagonistic relationships that cause negative frequency-dependent selection (e.g., host-pathogen interactions), individual genotypes face constantly deteriorating
environments. Little evidence directly supports this contention; however, I am prejudiced toward it, largely because of
the prevalence of sex and recombination in the life cycles of
long-lived organisms. All told, it is almost startling that so
few ecologists have attempted to articulate such a succinct,
yet comprehensive, list. What remains to be seen is how the
list will be broadened and refined (without becoming cumbersome), and whether the articulation of these properties will
point the way to a synthetic and quantitative theory that
relates ecological variation to evolutionary change (and vice
versa).
In the next chapter, Mary Jane West-Eberhard establishes
an intellectual link with Bonner by advancing the view that

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1604

REVIEWS

behavioral processes, like developmental processes, are "condition-sensitive." After reading the chapter several times, I
remain uncertain exactly what "condition-sensitive" means:
at times the term appears to refer to adaptive phenotypic
plasticity, in which the phenotype of an organism changes
(reversibly or not) in response to the environment. At other
times, "condition-sensitive" seems more inclusive, such that
phenotypic response (or phenotype, itself) depends on both
the condition of the organism and the condition of the environment. In turn, the condition of the organism depends
on the individual and collective properties of its genes, as well
as previous experience, nutritional status, etc. The adaptively
optimal phenotype may therefore vary according to the internal and external state of the organism. Whatever the correct
interpretation of "condition-sensitive," this ambiguity incited me to read further. The debatable heuristic foundation
of West-Eberhard's argument is that a new post-Darwinian
kind of typological thinking about species has replaced preDarwinian typology. The "old" typology held that species are
essentially phenotypically invariant; the "new" typology assumes that species vary, but the distribution of the variance
is unimodal and normal. As she puts the "new" dogma, "populations are unimodally adapted." She continues, "So, to get
two adaptive peaks, or modes, you must have a branch."
Thus, in the traditional wisdom, speciation is at the heart of
evolutionary novelty.
The rest of the chapter provocatively counters this notion
by drawing on West-Eberhard's elegant studies of wasps. Each
of these dazzling vignettes highlights behavioral flexibility and
developmental plasticity as intraspecific diversifying forces.
She cogently argues that the "switches" controlling the expression of "condition-sensitive traits" allow the dissociation
of complex sets of phenotypic alternatives across both ontogenetic and evolutionary time. Consequently, major evolutionary novelties can arise and be perpetuated within a species through "condition-sensitive" processes, and there is no
need to appeal to unknown sorts of genetic mechanisms to
account for major evolutionary transitions. As one of my
colleagues put it, "Imagine: no more slogging through adaptive valleys." The bottom line, one that begs to be explored
further, is that "condition-sensitive" processes do not merely
buffer the genotype against phenotypic and environmental
change, but provide the grist for all sorts of evolutionary
diversification.
Leo Buss and Matthew Dick present a picaresque and illuminating set of three bestiaries about worms, flies, and tunicates, each of which provocatively touches on the relationship between developmental processes and evolutionary
novelty and complexity. In contrast to the essay by WestEberhard, which examines the phenotypic origin of evolutionary novelty, the first two stories speculate on the genetic
basis of evolutionary novelty. Buss and Dick first tempt us
with a brief, but incisive, comparison of asexual propagation
in polychaetes (about which virtually nothing is known genetically) to the well-studied developmental genetics of segmentation in Drosophila. This was a jewel of a story-one
worth reading many times. It eloquently shows how developmental and molecular genetic studies, set in an imaginative
(and appropriate) comparative framework, can illuminate a
vast area of morphological mystery. They move on to pitch
saturation mutagenesis as a means to explore what is phenotypically "possible." I wish I had a clearer understanding
of the implications of "possible." My own view is that such
techniques may yield some information on what could evolve,

Ecology, Vol. 74, No. 5

but that the scope of evolutionary possibility revealed by

saturation mutagenesis ought to be rather limited. This is
partly because a number of often poorly understood developmental processes and improbable historical events surely
constrain the outcomes of any such genetic bombing runs. I
suspect there are epistemological problems, too. For instance,
how many rounds of saturation mutagenesis (plus, presumably, selection) on some lineage of ancestral protocirripedes
would be necessary to unleash the genotype and phenotype
of a barnacle? Can anyone imagine in retrospect, much less
in prospect, how the transformation occurred? In the final
story, Buss and Dick propose that the complex life cycles
characteristic of flatworm parasites, hydrozoan cnidarians,
and in the most fantastic cases, slime molds and pelagic tunicates, are the outcomes of conflicts between levels and units
of selection. In the case of slime molds, there is certainly the
potential for evolutionary conflict, because different genotypes can (and do) collaborate to form multicellular reproductive structures. I found the salp example less scrutable
because, barring somatic mutation, all of the components of
the organism (some of which clearly forego the production of
gametes) are genetically identical. Thus, one of the essential
elements for selection to occur, namely genetic variation, is
not an element of the series of composite organisms that
compose the life cycle of many pelagic tunicates. Still, the
extraordinary morphological and functional specialization
apparent in these life cycles calls out for some explanation,
but perhaps not a single explanation.
Marc Kirschner's chapter on the evolution of the cell starts
with still another controversial proposition: "Evolution is best
understood on the level of evolution of cellular processes."
However debatable this assertion might be, the implications
of the chapter go far beyond that idea, for this is the only
essay in the book that takes on what others treat as a metaphysical question: What are the mechanistic relationships between nucleic acid sequences, developmental processes, and
morphological change, and how have these relationships
evolved? He employs a simple and powerful computer metaphor to argue that over the history of life, cellular components are relatively unchanging hardware, and that novel gene
products arise relatively rarely. In contrast, software changesespecially those that involve integration and reorganization
of cellular elements-underlie most major evolutionary change.
As he puts it, "the truly great moments in evolution came
when operating systems, or collections of software, were created." The force that creates these software revolutions is
never clearly identified, but the metaphor remains a powerful
one, and reconciles well with the conservatism of basic cellular
structure. His conclusion-one that is reminiscent of WestEberhard's, but at a different level of organization: the mechanisms that integrate cellular processes have the evolved capacity to promote substantial evolutionary change with little
associated genetic change. Comparative developmental genetics once again moves to center stage.
Like Kirschner, Marty Kreitman surveys the, "intellectual
meeting ground for evolutionary biology and modern molecular biology." Kreitman tempers the euphoria of Kirschner's
essay, but he also surveys a very different part of the venue.
The first part of the chapter takes stock of the limitations of
the "molecular approach," particularly with respect to unravelling evolutionary process and phylogenetic pattern. In
Kreitman's final reckoning, it seems that molecular analyses
will reveal unprecedented amounts of information concerning
levels and patterns of genetic variation; his prognosis for using

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REVIEWS

July 1993

this information to unravel evolutionary process-at least

beyond the level of gene and genome structure-is trenchant
and humbling. To keep the balance, the essay then highlights
the empirical and theoretical constraints of evolutionary biology-even experimental studies on short-lived organismsto address some of the most basic process-oriented questions
(e.g., is allelic variation selectively neutral?). As he incisively
points out, part of the problem arises from limits to detection
of selection, making it difficult to reject either selectionist or
neutralist options. But, the problem appears to be deeper still,
as 'he documents with examples from his own work on Drosophila: when multiple processes contribute to evolutionary
change, how can the contribution of each be isolated? Although I think he overstates the problem when he asserts, "it
is formally impossible to distinguish between overdominant
selection and frequency-dependent selection," his cautions
are generally well-taken and should be well-heeded.
If you've been holding your breath awaiting the synthesis

1605

of neodarwinism, paleontology, development, and molecular

biology into a radical new framework for understanding evolution, or, even if you've just been hoping for an incisive
diagnosis and prescription for a unification of evolutionary
biology, Molds, molecules, and metazoa unavoidably falls short
of the mark. If, however, you are willing to do a little prospecting in a small book, there are real gems to be discovered.
At first sight, many of these gems seem small and uncut-the
kind that are easily passed over. But in the spirit of John
Bonner, the book compelled me to seek my colleagues for all
sorts of advice, to tread across alien ground, and to look at
familiar and baffling questions in unfamiliar ways.
RICK GROSBERG
UNIVERSITY OF CALIFORNIA

Center for Population Biology

Davis, California 95616

Ecology, 74(5), 1993, pp. 1605-1606

? 1993 by the Ecological Society of America

HIERARCHY AND UNITY IN ECOLOGY

Allen, T. F. H., and Thomas W. Hoekstra. 1992. Toward a

unified ecology. Columbia University Press, New York. xiv
+ 384 p. $45.00, ISBN: 0-231-06918-9.
An unusual view of ecology. The book provokes, illuminates, and twists perspective. It is important for those who
enjoy speculation, those who look for the meaning of their
work, and those who appreciate or oppose the role of general
abstract thinking in the development of ecology. Allen and
Hoekstra aim to provide a cohesive intellectual framework
for ecology, and especially ecological complexity. They accomplish this ambitious task in part only. A device which
they use to pursue the stated goal is to break current ecological
traditions, expose their weaknesses, and use the pieces to build
a different perspective.
The book's structure develops around five "criteria" or
traditional concepts of ecology-landscape, ecosystem, community, organism, and population. In an exhaustive discussion, richly illustrated by well-known case studies, Allen and
Hoekstra launch an all out attack on . . . (!) hierarchy. Their
main line of argument is that the traditional conceptions of
ecological hierarchy are untenable and an obstacle to a productive pursuit of ecology. They emphasize that each of these
conceptions has different properties, modes of description,
and research protocols. Thus, they argue, neither are landscapes generally composed of ecosystems, nor are populations
building blocks for communities. If there is a hierarchy, then
it is one of landscapes containing smaller landscapes, or populations containing sub-populations. In other words, Allen
and Hoekstra largely replace the "old hierarchy" with a within-criterion scaling.
Additionally, the book analyzes interactions among the five
criteria. To be effective at this, the authors, somewhat artificially, contrast ecosystems, communities, and landscapes.
Nevertheless, they succeed in showing, for example, how corridors, history, and disturbance link the landscape with the
community conception. Another tangible theme of the book

is a demonstration of how scale and hierarchical constraints

influence our ability to make specific ecological predictions.
What may be the most attractive aspect of the book from
the reader's point of view-a critique of the traditional understanding of the five criteria-is also a liability. By focusing
on current conceptions and by attempting to find connections
and differences among them, the authors become entangled
in terminological and empirical diversity and contradictory
evidence. Occasionally, this affects the logic of the presentation. For example, Allen and Hoekstra argue that there are
no real entities in ecology. By the way, I know of no scientific
criteria to distinguish real from non-real, or perhaps unreal,
entities and that all conceptual devices we use are of our own
making. However, they often refer to "natural" entities as
well as to "entities robust to transformations." These types
of entities are of great importance to ecologists because they
exhibit many consistent properties. If this is correct, and I
believe it is, such entities should be examined with more
scrutiny. The book does not suggest how we know which
conceptual devices reflect "natural entities" or "entities robust to transformations." It does not comment where these
entities are coming from, and what are the attributes that
make them natural or robust. This omission is deliberate.
Within the framework proposed by the authors, entities robust to transformations emerge from empirical experience
and that is it. But if the empirical experience leads to different
results, with some entities being feeble and some robust, should
we not try to develop ideas or theories that could account for
differences among them? The book leads then to the identification of one of the most general problems of ecology, even
if in an oblique way. Two criteria, high relative integrity and
persistence, distinguish "entities robust to transformations"
or, simply, things. These two criteria scale up or down in the
same fashion as any other discussed in the book. I believe
that they also are key to the development of unifying approaches. It is integrated things that aggregate into higher level
entities. Otherwise, scaling is merely an exercise in our perceptions.

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