Themes on Variation

Variation: A Central Concept in Biology. Benedikt Hallgrímsson and Brian K. Hall, eds. Elsevier Academic Press, Burlington, MA, 2005. 592 pp. $74.95 (ISBN 9780120887774 cloth).

Darwin's engine, natural selection, requires fuel to drive it, and variation among individuals provides this fuel. Our mechanistic understanding of how the engine operates to transform populations has been enhanced by theoretical and empirical studies in population and quantitative genetics over many years. However, until recently, despite countless studies amassing data on the quantity and quality of the requisite fuel, no parallel body of theory and experiment on the origins and maintenance of variation has arisen. Over the past decade, authors in a variety of disciplines have begun to develop frameworks for nderstanding these issues. The editors of Variation: A Central Concept in Biology, Benedikt Hallgrímsson (University of Calgary, Alberta, Canada) and Brian K. Hall (Dalhousie University, Halifax, Nova Scotia, Canada), bring together a group of experts with a view toward building on these frameworks. Their own contributions emphasize the distinction between variability (the predisposition to vary) and variation, and focus on understanding the forces generating three patterns of variation: canalization, developmental stability, and morphological–developmental integration.

Peter Bowler opens with a fine overview of the history of ideas concerning variation. He begins with Darwin's views and contrasts them with those of Darwin's contemporaries. He then details the changes in viewpoint that evolved en route to the subsequent synthesis. The next chapter is an update by Leigh Van Valen of his 1978 classic “The Statistics of Variation.” Following this section, chapters are loosely organized into three thematic areas: genetic and developmental determinants of variability, environmental determinants of variation, and comparative studies of variation.

Chapters by D. C. Jones and R. Z. German, Miriam Zelditch, and Ellen W. Larsen emphasize the importance of recognizing ontogenetic components of variation. Zelditch's chapter is noteworthy for her discussion of four biological hypotheses related to patterns of variation and canalization of skull shape: targeted growth, variation in developmental timing, modularity, and neural regulation. She provides a lucid presentation of the expected patterns and their causes, and the problems associated with distinguishing hypotheses that have overlapping predictions.

Canalization and constraint are covered in five chapters. Ian Dworkin contrasts what he refers to as two definitions of canalization, a reaction norm view and a variation view. He says that “at this point it is unclear which definition is in fact the correct one,” but I would argue that both the across-environment and the within-environment perspectives are valid. Dworkin also raises the important issue of cryptic variation (what I call “hidden reaction norms”) and discusses the issues of its genetic architecture and its role in evolution.

Hidden variation is again addressed by Ary A. Hoffman and John A. McKen-zie when they review the concept of evolutionary capacitors, or mechanisms for storing variation for future release. I was a bit surprised in this chapter at the section heading “Do we need variability generators?”which seemed to me to be the wrong question to ask. Instead, we should ask, “What proportion of evolutionary change can be attributed to different sources of variation?” (i.e., new mutations versus hidden variation). Alexander Badyaev addresses this issue more directly by examining the issue of stress-induced variation (using examples in bumblebees and shrews) and how it may be integrated and accommodated by the organism.

The flip sides of canalization—plasticity and developmental instability (noise, asymmetry)—also receive explicit coverage in several contributions (e.g., A. Richard Palmer's tour of antisymmetry). Sonia Sultan and Steve Stearns's exposition on reaction norms is notable because it goes beyond the standard treatment of plasticity to address more explicit developmental themes, and it raises questions about how genetic variation for plasticity within different species can affect community-level processes such as competition and predation.

The concluding essays outline three distinct perspectives on future research agendas, and their similarities and differences are revealing. For example Hallgrímsson and Hall explicitly identify three patterns of phenotypic variation—canalization, developmental stability, and morphological integration. Phenotypic plasticity is never mentioned in the chapter; it appears to be implicitly included within canalization. David M. Parichy echoes that view, calling plasticity a “breakdown in canalization,” but notes that it “has been profoundly understudied by mainstream developmental biology.” In contrast, Samuel Sholtis and Kenneth Weiss explicitly include responses to the environment in their framework for the study of phenogenetics (i.e., how genotypes map to phenotypes). In this context, they suggest the importance of a phenomenon they term “phenogenetic drift”: random changes in the genetic underpinnings of a specific phenotype. (This is akin to the idea of neutral networks discussed by Lauren Ancel Meyers earlier in the book; see also Ancel Meyers et al. 2005.) The result of this drift is that while phenotypes may change little or not at all, random genetic changes may be moving the organism toward other genetic boundaries where phenotypic change may be substantial. I agree that this is a key concept for our ultimate understanding of phenotypic evolution. Although Sholtis and Weiss's exposition of the many alternative routes between gene and phenotype may leave readers frustrated by the potential complexity, it is an accurate representation of the reality we need to accommodate.

One source of annoyance in this volume is the lack of a consistent terminology. Terms such as “canalization,” “epistasis,”and “developmental plasticity” are all used with multiple meanings. In some cases, individual authors take care to make their usages explicit, but in others it is clear that a different meaning is intended. A second peeve: I was nagged throughout this book by the glaring taxon bias. Zoologists (including anthropologists) wrote 20 of 22 chapters (including one that was coauthored with a botanist). This would pose no problems if there were no literature on variation in plants, fungi, and single-celled organisms (not so), or if the scholarship in the contributions extended to embrace the other literature. (In the most egregious example of exclusion, of 60 taxon-specified references in one conceptual chapter, 59 were to animals and only 1 to plants.)

As an overview and attempt at synthesis, I found the volume uneven. Reviews of developmental noise and antisymmetry get their own chapters, but mutation and recombination, topics that one might consider central to the study of variation and variability, are covered in five pages. Genetic and developmental sources of variability and variation get abundant coverage, but environmental sources seem marginalized. However, the majority of chapters are authoritative and well written, and graduate students and scientists will find much here that is thought-provoking.