Books and Arts

Nature 424, 16-17 (3 July 2003) | doi:10.1038/424016b

A flexible theory of evolution

Gerdien de Jong1 & Ross H. Crozier2

BOOK REVIEWEDDevelopmental Plasticity and Evolution

by Mary Jane West-Eberhard

Oxford University Press: 2003. 720 pp. $100, £79.50 (hbk); $49.95, £37.50 (pbk)

It is an ancient truism that what evolves is the developmental system, from which it follows that genetics, development and evolution are interwoven. Genetics and evolution were integrated long ago in the synthetic theory of evolution; development has only lately rejoined the evolutionary fold. The field of evolutionary developmental biology thus created is mostly concerned with patterns of evolution, comparing the genetic basis of evolutionary changes in development, rather than with the dynamics of evolutionary changes. Its sister, developmental evolutionary biology, studies how selection works on development to produce the adaptive phenotype, necessarily becoming linked to evolutionary ecology. This is a field worth pursuing, and Mary Jane West-Eberhard's Developmental Plasticity and Evolution certainly belongs within it, but the question is whether the book does the field good service.

For West-Eberhard the phenotype is central. But this is not the bleak 'genotype + environment = phenotype' taught to first-year students, but rather a vibrant, living, changing phenotypic whole, far from dreary genetic determinism. The phenotype is developmentally plastic, changing in many ways in response to many environmental challenges. To be alive is to be developmentally plastic. West-Eberhard envisages a synthetic theory of evolution and development in which environmentally induced phenotypic change gives rise to adaptive evolution as readily as, or even more readily than, mutationally induced phenotypic change.

The main evolutionary process, in West-Eberhard's universe, involves environmental change, phenotypic accommodation and genetic accommodation. An environmental change elicits a developmentally plastic response, and phenotypic accommodation — the immediate adjustment to a change resulting from the multidimensional adaptive flexibility of the phenotype — ameliorates its harm to individuals. New phenotypes resulting from this developmental plasticity are selected. A change in allele frequency — genetic accommodation — improves and incorporates the change. In this way the environment becomes a crucial participant in the generation and selection of adaptive design.

In West-Eberhard's view, this sequence of developmental plasticity, phenotypic accommodation and genetic accommodation is the mechanism responsible for (nearly) all evolutionary novelty, adaptive radiation, speciation and macroevolution. Evolution proceeds through adaptive developmental phenotypic plasticity.

Mainstream evolutionary biology is riddled with genetic determinism, blocking a biological view of the organic phenotype, West-Eberhard suggests. However, many of the biological studies she adduces in her support belong to the mainstream. Nobody objects to "a unified Darwinian theory that relates developmental plasticity to genetic change", but it is a matter of proportion. West-Eberhard sees too much unwarranted emphasis on genes; many will see an unwarranted role for developmental plasticity in her argument, as the description of phenotypic plasticity itself is too general and vague to get to grips with.

West-Eberhard's conviction of the primacy of the environment as the inducer of new phenotypic variation runs through the book, making her ask for a coherent evolutionary theory that uncompromisingly includes the environment alongside the genome in all aspects of evolutionary thought. She accepts that genetic change accompanies evolution, but only as genetic accommodation follows environmental induction; evolution as genetic change "is left hanging by a tenuous thread". In this view, genes are followers, not leaders.

How plausible is all this? Not very. No convincing evidence is presented for adaptive phenotypic accommodation to a new environment. Genetic accommodation is just a classical adaptive change in gene frequency. Developmental plasticity exists and is important in nature, but for it to be the dominant evolutionary factor, one has to show that developmental plasticity is predominantly adaptive and precedes genetic adaptation.

West-Eberhard refers to much good biology, but fails on the major point: developmental plasticity as the initiating factor of adaptive novelty preceding genetic change. The evidence shows that much developmental plasticity exists and has a genetic basis, no more and no less. West-Eberhard concedes that direct examples of adaptive environmental induction are lacking, but she labels many cases as indirect evidence reflecting the process. Whether the environment is the main player in eliciting adaptive developmental plasticity, and thereby in all other evolutionary processes, remains a question of faith. No crucial laboratory experiment is suggested that would test whether environmental induction leads to adaptive evolution. Actually, some tests for phenotypic accommodation (as 'beneficial acclimation') have been done by Raymond Huey's group at the University of Washington, and were negative.

In one of the first studies of phenotypic plasticity, Richard Woltereck defined the reaction norm as the range of the phenotypes that an individual could exhibit over all environments. The original insight was: "Genotypus = Reaktionsnorm", the genotype being the information for developmental plasticity. Woltereck transplanted Daphnia from Denmark to Italy to investigate whether the environment modified the reaction norm: it didn't. Later, dissatisfied with 'materialism' but impressed with phenotypic plasticity, Woltereck wrote two books, unfortunately incomprehensible, expressing a holistic view. In reading West-Eberhard's Developmental Plasticity and Evolution, one also often struggles with the verbal arguments: what does this mean, and how, precisely, would that work? West-Eberhard asserts a vision but presents little analysis. A major new synthesis and research programme this book is not.

  1. Gerdien de Jong is in the Department of Evolutionary Population Biology, Utrecht University, Padualaan 8, NL-3584 CH Utrecht, the Netherlands
  2. Ross H. Crozier is in the Department of Evolutionary Genetics, School of Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia.