Carl D. Schlichting

Adaptive phenotypic plasticity: consensus and controversy.

Phenotypic plasticity is an environmentally based change in the phenotype. Understanding the evolution of adaptive phenotypic plasticity has been hampered by dissenting opinions on the merits of different methods of description, on the underlying genetic mechanisms, and on the way that plasticity is affected by natural selection in a heterogeneous environment. During much of this debate, the authors of this article have held opposing views. Here, we attempt to lay out current issues and summarize the areas of consensus and controversy surrounding the evolution of plasticity and the reaction norm (the set of phenotypes produced by a genotype over a range of environments).

Phenotypic plasticity's impacts on diversification and speciation

Phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) is commonplace. Yet its evolutionary significance remains controversial, especially in regard to whether and how it impacts diversification and speciation. Here, we review recent theory on how plasticity promotes: (i) the origin of novel phenotypes, (ii) divergence among populations and species, (iii) the formation of new species and (iv) adaptive radiation. We also discuss the latest empirical support for each of these evolutionary pathways to diversification and identify potentially profitable areas for future research. Generally, phenotypic plasticity can play a largely underappreciated role in driving diversification and speciation.

Phenotypic plasticity and evolution by genetic assimilation

SUMMARY In addition to considerable debate in the recent evolutionary literature about the limits of the Modern Synthesis of the 1930s and 1940s, there has also been theoretical and empirical interest in a variety of new and not so new concepts such as phenotypic plasticity, genetic assimilation and phenotypic accommodation. Here we consider examples of the arguments and counter-arguments that have shaped this discussion. We suggest that much of the controversy hinges on several misunderstandings, including unwarranted fears of a general attempt at overthrowing the Modern Synthesis paradigm, and some fundamental conceptual confusion about the proper roles of phenotypic plasticity and natural selection within evolutionary theory.

Phenotypic Integration and Environmental ChangeWhat are the consequences of differential phenotypic plasticity of traits

nformation on developmental processes is now being incorporated into theories of the evolution of phenotypic characteristics (Cheverud 1984, Lande 1982). Such theories typically focus on the developmental trajectory expressed in a single environment. But biologists have recently recognized the need to incorporate developmental flexibility in multiple environmental conditions into evolutionary theories (Schlichting 1986, Stearns and Koella 1986, Sultan 1987, Via and Lande 1985). Phenotypic plasticity, the morphological and physiological responses of an organisms phenotype to a change in environmental conditions, represents the interplay between ecological factors and the developmental program of the organism. Some plastic responses are obviously adaptive, but answers to questions concerning the way in which adaptive plasticity and norms of reaction evolve are elusive (Via 1988). What does a plastic response of a trait involve? Some plastic responses may simply be changes in scale, as for example when plants simply grow less when they lack nutrients. But how much growth is stunted under the same conditions can vary among genotypes. Such differences in phenotypic plasticity represent genetic differences in their developmental programs. Other types of plastic response may Heterogeneous environments favor the

Gene regulation, quantitative genetics and the evolution of reaction norms

SummaryThe ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.

Hidden Reaction Norms, Cryptic Genetic Variation, and Evolvability

There is reason to suspect that hidden reaction norms (variation that is phenotypically expressed only after changes in internal or external environmental conditions) may store an evolutionarily significant pool of cryptic genetic variation upon which selection may act. I review mechanisms that may hide variation and the processes that can release this variation. I discuss the potential significance of cryptic genetic variation and elaborate on an example where the release of such variation initiated the evolution of the genetic architecture of multicellular organisms.

Reaction norms of Arabidopsis. I. Plasticity of characters and correlations across water, nutrient and light gradients

The univariate and multivariate study of variation for phenotypic plasticity is central to providing a clear understanding of hypotheses about the genetic control and evolution of reaction norms in natural populations. Arabidopsis thaliana is an ideal organism for the study of Genotype × Environment interactions (i.e., genetic variation for plasticity), because of the ease with which it can be grown in large numbers and due to the amount of information already available on its genetics, physiology and developmental biology. In this paper, we report on the plasticity, genetic variation and G × E interactions of four populations of A. thaliana in response to three environmental gradients (water, light and nutrients), each characterized by four levels of the controlled parameter. We measured nine traits and obtained their reaction norms. Path analysis was used to study the plasticity of character correlations. We found a tendency for A. thaliana reaction norms to be linear (either flat, i.e. no plasticity, or with a significant slope), in accordance with previous studies. We detected substantial amounts of genetic variation for plasticity in the light and nutrient gradients, but not in the water gradient. Dramatic restructuring of character correlations was induced by changes in environmental conditions, although some paths tended to be stable irrespective of the environment, thereby suggesting some degree of canalization.

Phenotypic plasticity in Phlox

SummaryThree species of Phlox (Polemoniaceae) were grown in 6 greenhouse treatments. A variety of traits were recorded and the correlations among them were computed for each treatment. The phenotypic correlations between characters are significantly altered when plants are grown under different environmental conditions. These changes in correlation structure result from the differential phenotypic plasticity of traits. Partial correlations between flower production and other traits are also environment-dependent. Such changes can alter the intensity of, and possibly the response to, selection on traits correlated with fitness in natural plant populations.

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity’s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.

Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation.

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.