Phenotypic Plasticity: Functional and Conceptual Approaches. Thomas J. DeWitt and Samuel M. Scheiner, eds. Oxford University Press, New York, 2004. 247 pp., illus. $59.95 (ISBN 0195138961 cloth).
Understanding the evolution of phenotypic plasticity—the environmental induction of phenotypic change owing to altered gene expression—will conceptually unify development, physiology, immunology, and endocrinology. Each of these disciplines uses different terminology to describe phenomena related to plasticity. The editors of Phenotypic Plasticity: Functional and Conceptual Approaches—Thomas J. DeWitt, of Texas A&M University, and Samuel M. Scheiner, who works for the National Science Foundation—have brought together a diverse set of approaches to update the state of plasticity research.
The historical chapter by Sarkar (chap. 2) provides a lucid description of key historical issues framing current scientific debates. In particular, debates on plasticity in the 1990s sharpened semantic definitions, allowing a conceptual consensus to emerge. The chapter brings any reader up to speed on key theoretical issues, particularly when followed by the chapters on theory (chap. 6, by Berrigan and Scheiner; chap. 7, by Dewitt and Langerhans; chap. 11, by Wolf and colleagues). Are there “genes for plasticity,” a view championed by Scheiner and colleagues, or does selection arise from a “byproduct of selection on trait means,” a view championed by Via? A key issue to emerge from this dialectic is the role of epistatic effects. As noted in the chapters that review theory (chaps. 2, 6, 7, and 11), models rarely include epistatic interactions, although there are some notable exceptions.
What are the true genetic underpinnings of plasticity? A hierarchical description of genetic effects includes allelic sensitivity, dominance sensitivity, and epistatic sensitivity to the environment. Allelic and dominance sensitivity are easy to visualize, and several of the theoretical chapters provide models incorporating such genetic variation. Epistatic sensitivity is more difficult to grasp. The simplest way, and that adopted in much of the current theory, is to visualize epistasis arising from “regulatory loci that exert environmentally dependent control over structural gene expression” (Schlichting and Pigliucci , cited in chap. 2). A more general perspective is that afforded by the theory of indirect genetic effects (chap. 11), which allows for gene interactions arising both within and between genomes. At a mechanistic level, however, there exists a myriad of interactions among structural, physiological, hormonal, or developmental genes, as well as immunological gene complexes (both within and between individuals), not just interactions from regulatory loci. Whether a simplified approach to regulatory-locus epistasis is justified remains an open question to be resolved by empirical approaches.
Despite the simplifications in the theory regarding epistasis, identifying links to regulatory loci is an important first step in empirical analysis, because it is amenable to the “candidate-gene approach” (chap. 5, by Frankino and Raff). The candidate-gene approach is epitomized by work on plant elongation owing to phytochromes. Plants elongate their stems in response to the red-to-farred (RFR) ratio of light (cited in chap. 10, by Dudley), and RFR can be manipulated in many environmental treatments. Shading due to plant density causes a shift in RFR ratios and thereby induces the adaptive response of stem elongation. In animals, a similar candidate gene involves regulatory genes of stress, such as corticotropin-releasing hormone, which triggers the release of glucocorticoid steroid hormones (chap. 5). This in turn induces a variety of plastic responses in vertebrates.
However, as noted above, epistasis could arise from any kind of gene interaction, not just from regulatory loci. To move beyond the candidate gene, plasticity research must adopt genomic approaches, as advocated in two chapters (chap. 5, by Frankino and Raff, and chap. 13, by Scheiner and DeWitt). Genomics, which currently involves linkage mapping or screening with gene chips, remains a daunting task, given that gene interactions must be screened in a variety of biotic and abiotic environments. Perhaps model systems such as Drosophila (discussed in chap. 4, by David and colleagues) may be useful in implementing genomic approaches, given the extraordinary detail afforded by current genetic maps and gene sequences. However, many issues involving the adaptive costs of plasticity and natural selection on plastic responses can be resolved only in the wild. Thus, genomic approaches will ultimately need to be implemented in natural systems to fully understand the genomic architecture of plasticity.
In addition to proximate issues, contributors to the volume do discuss adaptive issues, such as costs of plasticity, tradeoffs, and adaptive value (chap. 9, by Doughty and Reznick). To date, no study has measured the fitness consequences of plasticity in nature (i.e., the effects of induced plasticity on the production and survival of offspring); only proxies for lifetime reproductive success have been assessed. Information on actual fitness consequences is essential to comprehensively assess costs and tradeoffs. Other theoretical chapters (chaps. 6 and 7) highlight neglected areas of empirical research, such as the temporal or spatial prevalence of inducing cues. Furthermore, as Sih points out in chapter 8, the social induction of plasticity is rarely treated in a frequency-dependent context. Behavioral ecology and game theory explicitly treat frequency dependence and the cues for inducing adaptive plasticity. Incorporating such frequency dependence will advance the study of plasticity in social systems. The plasticity of mating systems is often linked to traits with direct fitness effects.
Furthermore, game theory provides a number of examples of cyclical dynamics that involve recurring environments. Plasticity should be strongly favored in such varying or cyclical social contexts. Chapter 11 treats the theory of social contexts, but completely ignores frequency-dependent effects. Instead, a quantitative genetic analysis is used to focus, gene by gene, on the important consequences of gene–environment interactions for linkage disequilibrium, pleiotropy, and the formation of genetic correlations. However, frequency dependence and the spatial scale of nearest-neighbor interactions will often strengthen the formation of genetic correlations arising from linkage disequilibrium. Thus, a comprehensive treatment of the evolution of plasticity involving biotic interactions will require an explicit analysis of frequency dependence in conspecifics' interactions and in plant–herbivore, predator–prey, and host–parasite coevolutionary relationships.
There are other neglected adaptive issues. The role of settlement behavior as a correlating force between genes, environment, adaptive response, and ensuing assortative mating is impossible to test in most laboratory settings. An analogous force in plants would be plant-mediated dispersal of seeds by animals or extremely strong microhabitat-dependent selection, which might also strengthen genetic correlations. These forces might be crucial in future models of speciation driven by the evolution of plasticity.
The volume does include a chapter, by Schlichting (chap. 12), on the role of plasticity in diversification and speciation. Ultimately, a theory about this role will require the rigor found in current genetic models of speciation, and this has not yet been achieved. But this chapter does provide a number of potential genetic mechanisms, such as genetic assimilation, that could be modeled in the future. While the chapter is far too short to sketch out the full problem of phenotypic plasticity, it does serve as a useful abstract of ideas on the subject. These ideas are more fully developed in Mary Jane West-Eberhard's (2003) recent tome, which treats speciation driven by plasticity.
In summary, DeWitt and Scheiner's volume provides a useful summary of current work and future directions for the field. As such, it should be on the shelf of evolutionary ecologists, whatever their specialty (genetics, physiology, endocrinology, or behavior). The editors admit that the field is in a phase of logarithmic increase (chap. 13), with much work yet to be done. I am sure the book will recruit more researchers to plasticity research. Many chapters in the volume are excellent, and must-read material for both established scientists and new students of plasticity.