An alternative evolutionary synthesis

Sinauer, 1998. £29.95 pbk (xii + 387 pages)ISBN 0 87893 799 4One of the most important conceptual breakthroughs of contemporary evolutionary biology has been the widespread recognition of the prominent role of internal, or structural, features of organisms in mediating a wide range of fundamental phenomena, including the origin of morphological novelty, the integrated evolution of complex characters, and even the differential success and diversification of lineages. Although relevant internal features can range from sheer physical attributes and the mechanical properties of biomaterials to functional (physiological) relationships, arguably the most prominent focus of current research is development. Phenotypic Evolution is the latest in a spate of single- and double-authored volumes1xThe Shape of Life: Genes, Development and the Evolution of Animal Form. Raff, R.A. See all References, 2xSee all References, 3xEvolutionary Developmental Biology (2nd edn). Hall, B.K. See all References, 4xThe Origin of Animal Body Plans: a Study in Evolutionary Developmental Biology. Arthur, W. CrossrefSee all References that attempt to address the inadequacy of the neodarwinian synthesis vis-a-vis the role of development5xHamburger, V. : 97–112See all References, 6xGilbert, S.F., Opitz, J.M., and Raff, R.A. Dev. Biol. 1996; 173: 357–372Crossref | PubMed | Scopus (364)See all References, by promoting more prominent incorporation of developmental approaches into the current evolutionary paradigm.The particular twist offered by Schlichting and Pigliucci is to promote the idea of the developmental reaction norm (DRN) as an important conceptual organizing principle for unraveling the many remaining mysteries of phenotypic evolution. The DRN has three key components: changes in ontogenetic trajectories, correlations among characters, and responses to different environmental conditions. It is inextricably linked to the environment and environmental variation, and Schlichting and Pigliucci unabashedly attribute inspiration for their ideas to the pioneering studies of ecogeographic variation by Clausen, Keck and Hiesey, as well as to the concepts of stabilizing selection and genetic assimilation as originally formulated by Schmalhausen, the great Russian morphologist, and Waddington, the British embryologist, among others. Their treatment comprises ten chapters. The first five present an introduction and background to the problem, along with overviews of the three key components of the DRN. The last half of the book applies ‘reaction norm thinking to problems in phenotypic evolution’. I enjoyed parts of the first section, especially the historical recapitulation; it's always rewarding to discover the depth, breadth and complexity of the ideas of our early intellectual heroes. How many people working in ‘evo-devo’ today, for example, know that J.M. Baldwin, who was among the first darwinians to propose a plausible mechanism for the evolution of phenotypic novelties (the ‘Baldwin effect’), published a book entitled Development and Evolution in 1902?Phenotypic Evolution, however, is not simply a summary of facts or an attempted ‘state of the art’ review. Instead, it explicitly promotes a research program for addressing an array of topics, ranging from organismal integration and constraints to the mechanisms of constructing the genetic architecture, to modes of evolutionary change and the origin of evolutionary novelties. The authors appropriately emphasize the role and ability of the environment to elicit phenotypic change, as well as the intrinsic capacity of existing developmental systems to produce novel features following a minor genetic or environmental perturbation. This message is too often lost, or at least minimized, in the frequent attention paid to dramatic phenotypic effects produced in gene-knockout experiments or overexpression studies. Their discussion of hidden variability also nicely presages the recent exciting report of this phenomenon following perturbation of heat-shock protein Hsp90 in Drosophila7xRutherford, S.L. and Lindquist, S. Nature. 1998; 396: 336–342Crossref | PubMed | Scopus (1289)See all References7. Finally, it is refreshing to see genetic assimilation resurrected as an important mechanism in the origin and stabilization of novel phenotypes – ‘it is the most likely mode of evolutionary change for many characters’ – although I wish that this theme had been developed further.Most authors of books in the field of evolution and development come from backgrounds in either paleobiology (or some other ‘macroevolutionary’ discipline) on the one hand, or molecular, cell and developmental biology on the other. In this light, the population- and quantitative-genetics perspective offered by Schlichting and Pigliucci is both valuable and welcome. It allows them, for example, to address a series of topics that receive little or no notice in other treatments; these include adaptation, phenotypic plasticity, heritability, environmental effects and heterogeneity, and genetic correlations. Nevertheless, this perspective does appear to come at a cost. For instance, as one who has come to regard allometry as principally a morphological or physiological concept, I was surprised (and somewhat chagrined) to see allometry (Chapter 4) defined much more broadly to encompass ‘the relationships among any phenotypic characteristics.’ Similarly, I was disappointed to see the treatments of two essential topics – constraints (Chapter 6) and phenotypic integration (Chapter 7) – focus so heavily on genetic correlations and/or covariance matrices, seemingly at the expense of other key aspects. Such a standardized, generic approach risks eliminating the dynamism of developmental and functional systems, the valuable idiosyncratic properties of specific characters and character complexes, and the potentially important role of other biological processes, all of which could contribute significantly to our understanding of constraints and integration.Phenotypic Evolution takes a different approach to the study of the relationship between development and evolution from that currently employed by many of its main practitioners. In many respects, it is a broader approach; for example, Schlichting and Pigliucci are not just interested in how novel phenotypes arise, but also in how they come to be established in populations and integrated into existing functional and developmental systems. Such an approach ultimately must prevail if modern biology is to achieve a truly synthetic understanding of evolution.