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Toward a Postmodern Synthesis Molds, Molecules, and Metazoa: Growing Points in Evolutionary Biology by Peter

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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Ecology, 74(5), 1993, pp. 1603-1605 C) 1993 by the Ecological Society of America




Grant, Peter R., and Henry S. Horn (eds.). 1992. Molds, molecules, and metazoa: growing points in evolutionary biol- ogy. 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 devel- opmental 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 evo- lutionary biology.

Molds, molecules,and metazoa. growingpoints in evolu-

tionary biology contains a series of essays derived from a symposium to celebrate the career of John Bonner. The ed- itors 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, mor- phological, and molecular perspectives. The first of the six "prospective" chapters, by James Val- entine, 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 collab- orate 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 diag- nostic attributes of major taxa that could explain macroevo- lutionary 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 sto- chasticity (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 (Mat- thew) and its relationship to the polychaete Canadia spinosa Walcott. Paleobiology 16:287-303). On the other hand, with- out an elaboration of why they resist extinction, Valentine's conclusion that the taxa which come to dominate the bio- sphere 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 microevolution- ary 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 theo- retical foundation of population genetics. In response, Bell sets out to elaborate a set of five "properties" of the environ- ment 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 environ- ments. In short, it states that genotype by environment in- teractions are so pervasive that norms of reaction of different genotypes often cross; consequently, fitness rankings of par- ticular genotypes should often change across selective regimes. The fourth property acknowledges that environments them- selves 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 impor- tantly, in his view) antagonistic relationships that cause neg- ative frequency-dependent selection (e.g., host-pathogen in- teractions), individual genotypes face constantly deteriorating environments. Little evidence directly supports this conten- tion; 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,

list. What remains to be seen is how the

list will be broadened and refined (without becoming bersome), 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

yet comprehensive,


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Ecology, Vol. 74, No. 5

behavioral processes, like developmental processes, are "con- dition-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 en-


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 in- ternal and external state of the organism. Whatever the correct interpretation of "condition-sensitive," this ambiguity in- cited 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 pre- Darwinian typology. The "old" typology held that species are essentially phenotypically invariant; the "new" typology as- sumes that species vary, but the distribution of the variance is unimodal and normal. As she puts the "new" dogma, "pop- ulations 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 ex-

pression of "condition-sensitive

of complex sets of phenotypic alternatives across both on- togenetic and evolutionary time. Consequently, major evo- lutionary novelties can arise and be perpetuated within a spe- cies 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 adap- tive 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 il- luminating set of three bestiaries about worms, flies, and tu- nicates, each of which provocatively touches on the relation- ship between developmental processes and evolutionary novelty and complexity. In contrast to the essay by West- Eberhard, which examines the phenotypic origin of evolu- tionary 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 ge- netically) to the well-studied developmental genetics of seg- mentation in Drosophila. This was a jewel of a story-one worth reading many times. It eloquently shows how devel- opmental 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 phe- notypically "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,

In turn, the condition

of the organism depends

traits" allow the dissociation

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 devel- opmental 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, presum- ably, 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 tu- nicates, 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 geno- types can (and do) collaborate to form multicellular repro- ductive 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 meta- physical question: What are the mechanistic relationships be- tween nucleic acid sequences, developmental processes, and morphological change, and how have these relationships evolved? He employs a simple and powerful computer met- aphor to argue that over the history of life, cellular compo- nents are relatively unchanging hardware, and that novel gene products arise relatively rarely. In contrast, software changes- especially 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 cre- ated." 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 West- Eberhard's, but at a different level of organization: the mech- anisms that integrate cellular processes have the evolved ca- pacity to promote substantial evolutionary change with little associated genetic change. Comparative developmental ge- netics once again moves to center stage. Like Kirschner, Marty Kreitman surveys the, "intellectual meeting ground for evolutionary biology and modern molec- ular 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 un- ravelling 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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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 bi- ology-even experimental studies on short-lived organisms- to 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 Dro- sophila: when multiple processes contribute to evolutionary change, how can the contribution of each be isolated? Al- though 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

of neodarwinism, paleontology, development, and molecular biology into a radical new framework for understanding evo- lution, 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 pros- pecting 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.


Center for Population Biology Davis, California 95616


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

? 1993 by the Ecological Society of America



Toward a

unified ecology. Columbia University Press, New York. xiv

+ 384 p. $45.00,

Allen, T. F. H., and Thomas W. Hoekstra.


ISBN: 0-231-06918-9.

An unusual view of ecology. The book provokes, illumi- nates, 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

complish 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.

around five "criteria" or

traditional concepts of ecology-landscape, ecosystem, com- munity, organism, and population. In an exhaustive discus-

sion, richly illustrated by well-known case studies, Allen and

(!) hierarchy. Their


ecological hierarchy are untenable and an obstacle to a pro- ductive pursuit of ecology. They emphasize that each of these conceptions has different properties, modes of description,

and research protocols. Thus, they argue, neither are land- scapes 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 pop-

ulations containing sub-populations. In other words, Allen and Hoekstra largely replace the "old hierarchy" with a with- in-criterion scaling. Additionally, the book analyzes interactions among the five criteria. To be effective at this, the authors, somewhat arti- ficially, contrast ecosystems, communities, and landscapes. Nevertheless, they succeed in showing, for example, how cor- ridors, history, and disturbance link the landscape with the community conception. Another tangible theme of the book

main line of argument is that the traditional conceptions

Hoekstra launch an all out attack on


They ac-

The book's

structure develops



is a demonstration

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 un- derstanding 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 presenta- tion. 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 ro- bust 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 ro- bust 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 identi- fication 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 ap- proaches. It is integrated things that aggregate into higher level entities. Otherwise, scaling is merely an exercise in our per- ceptions.

of how scale and hierarchical constraints

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