How stress selects for reversible phenotypic plasticity

Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays. The selective advantage of genotypes that are able to produce adaptive reversible plastic phenotypes is calculated by using the concept of environmental tolerance. Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non-induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions.     

The evolution of molecular biology into systems biology

Systems analysis has historically been performed in many areas of biology, including ecology, developmental biology and immunology. More recently, the genomics revolution has catapulted molecular biology into the realm of systems biology. In unicellular organisms and well-defined cell lines of higher organisms, systems approaches are making definitive strides toward scientific understanding and biotechnological applications. We argue here that two distinct lines of inquiry in molecular biology have converged to form contemporary systems biology.     

How caterpillars avoid overheating: behavioral and phenotypic plasticity of pipevine swallowtail larvae

We tested the hypothesis that larvae of the pipevine swallowtail butterfly, Battus philenor, employ behavioral and phenotypic plasticity as thermoregulatory strategies. These larvae are phenotypically varied across their range with predominantly black larvae (southeastern USA and California) and red larvae (western Texas, Arizona) occurring in different regions. Two years of field observations in south Texas indicate that the proportion of red larvae increases with increasing daily temperatures as the growing season progresses. Larvae were also observed to shift their microhabitats by climbing on non-host vegetation and avoided excessive heat in their feeding microhabitat. Larvae of ten half-sib families from populations in south Texas and California, reared under different temperature regimes in common garden experiments, exhibited plasticity in larval phenotype, with larvae from both populations producing the red phenotype at temperatures greater than 30°C and maintaining the black phenotype at cooler temperatures. However, larvae from Texas were more tolerant of higher temperatures, showing no decrease in growth rate in the highest temperature (maximum seasonal temperature) treatment, compared to the California population. In a field experiment, black larvae were found to have higher body temperatures when exposed to sunlight compared to red larvae. These results suggest that microhabitat shifts and the color polyphenism observed in pipevine swallowtail larvae may be the adaptive strategies that enable larvae to avoid critical thermal maximum temperatures.     

Evolutionary role of phenotypic plasticity

Phenotypic plasticity, i.e., the ability of a genotype to produce various phenotypes in response to changes in the environment, plays an important, although poorly understood and often underestimated, role in evolution. Both adaptive and nonadaptive phenotypic plasticity modulate the strength and direction of selection acting on a population and can, depending on conditions, either accelerate or inhibit adaptation, divergence, and speciation. Phenotypic plasticity also affects the direction of evolutionary change, which can either coincide with the direction of plastic changes (genetic assimilation) or be the opposite (genetic compensation). A special case of phenotypic plasticity is phenotypic change of the host caused by changes in its symbiotic microbiota. In the current review, we discuss the main forms of phenotypic plasticity and the current data on their impact on the rate and direction of evolutionary change. Special attention is paid to the results of recent experimental work, including the long-term evolutionary experiment on Drosophila melanogaster, which is being held at the Department of Evolutionary Biology, School of Biology, Moscow State University.     

Ecological consequences of phenotypic plasticity

Phenotypic plasticity is widespread in nature, and often involves ecologically relevant behavioral, physiological, morphological and life-historical traits. As a result, plasticity alters numerous interactions between organisms and their abiotic and biotic environments. Although much work on plasticity has focused on its patterns of expression and evolution, researchers are increasingly interested in understanding how plasticity can affect ecological patterns and processes at various levels. Here, we highlight an expanding body of work that examines how plasticity can affect all levels of ecological organization through effects on demographic parameters, direct and indirect species interactions, such as competition, predation, and coexistence, and ultimately carbon and nutrient cycles.     

Rethinking phenotypic plasticity and its consequences for individuals,populations and species

Much research has been devoted to identify the conditions under which selection favours flexible individuals or genotypes that are able to modify their growth, development and behaviour in response to environmental cues, to unravel the mechanisms of plasticity and to explore its influence on patterns of diversity among individuals, populations and species. The consequences of developmental plasticity and phenotypic flexibility for the performance and ecological success of populations and species have attracted a comparatively limited but currently growing interest. Here, I re-emphasize that an increased understanding of the roles of plasticity in these contexts requires a ‘whole organism'' (rather than ‘single trait'') approach, taking into consideration that organisms are integrated complex phenotypes. I further argue that plasticity and genetic polymorphism should be analysed and discussed within a common framework. I summarize predictions from theory on how phenotypic variation stemming from developmental plasticity and phenotypic flexibility may affect different aspects of population-level performance. I argue that it is important to distinguish between effects associated with greater interindividual phenotypic variation resulting from plasticity, and effects mediated by variation among individuals in the capacity to express plasticity and flexibility as such. Finally, I claim that rigorous testing of predictions requires methods that allow for quantifying and comparing whole organism plasticity, as well as the ability to experimentally manipulate the level of and capacity for developmental plasticity and phenotypic flexibility independent of genetic variation.     

Costs and limits of phenotypic plasticity

The costs and limits of phenotypic plasticity are thought to have important ecological and evolutionary consequences, yet they are not as well understood as the benefits of plasticity. At least nine ideas exist regarding how plasticity may be costly or limited, but these have rarely been discussed together. The most commonly discussed cost is that of maintaining the sensory and regulatory machinery needed for plasticity, which may require energy and material expenses. A frequently considered limit to the benefit of plasticity is that the environmental cues guiding plastic development can be unreliable. Such costs and limits have recently been included in theoretical models and, perhaps more importantly, relevant empirical studies now have emerged. Despite the current interest in costs and limits of plasticity, several lines of reasoning suggest that they might be difficult to demonstrate.     

Promising directions in plant phenotypic plasticity

A research agenda for the next phase of plasticity studies calls for contributions from a diverse group of biologists, working both independently and collaboratively, to pursue four promising directions: examining dynamic, anatomical/architectural, and cross-generational plasticity along with simpler growth traits; carefully assessing the adaptive significance of those plasticity patterns; investigating the intricate transduction pathways that lead from environmental signal to phenotypic response; and considering the rich environmental context of natural systems. Progress in these areas will allow us to address broad and timely questions regarding the ecological and evolutionary significance of plasticity and the nature of phenotypic determination.     

Ecological limits to plant phenotypic plasticity

Phenotypic plasticity is considered the major means by which plants cope with environmental heterogeneity. Although ubiquitous in nature, actual phenotypic plasticity is far from being maximal. This has been explained by the existence of internal limits to its expression. However, phenotypic plasticity takes place within an ecological context and plants are generally exposed to multifactor environments and to simultaneous interactions with many species. These external, ecological factors may limit phenotypic plasticity or curtail its adaptive value, but seldom have they been considered because limits to plasticity have typically addressed factors internal to the plant. We show that plastic responses to abiotic factors are reduced under situations of conservative resource use in stressful and unpredictable habitats, and that extreme levels in a given abiotic factor can negatively influence plastic responses to another factor. We illustrate how herbivory may limit plant phenotypic plasticity because damaged plants can only rarely attain the optimal phenotype in the challenging environment. Finally, it is examined how phenotypic changes involved in trait-mediated interactions can entail costs for the plant in further interactions with other species in the community. Ecological limits to plasticity must be included in any realistic approach to understand the evolution of plasticity in complex environments and to predict plant responses to global change.     

Origins of differentiation via phenotypic plasticity

How cell types of multicellular organisms came to be differentiated is still an open issue. Here I offer a model that posits that the origins of some cell differentiation patterns were originally passive outcomes of environmental effects. As cells' contact with the external environment was diminished, their patterns of gene expression were altered, due to changes in concentrations of externally supplied substances. Later, as multicellular growth continued, the relationships of cell layers to each other shifted, producing concentration gradients of signaling molecules. These gradients emanated both from the external cell layer toward the inside and from internal cell layers to adjacent layers. In this scenario then, differentiation arose initially as a by-product of the changing patterns of gene expression and of the complex mixtures and changing concentrations of substances passing among layers. Subsequent selection would operate to stabilize the expression patterns in those cell layers whose phenotypes provide a fitness advantage to the organism.     

Endocrine regulation of predator-induced phenotypic plasticity

Elucidating the developmental and genetic control of phenotypic plasticity remains a central agenda in evolutionary ecology. Here, we investigate the physiological regulation of phenotypic plasticity induced by another organism, specifically predator-induced phenotypic plasticity in the model ecological and evolutionary organism Daphnia pulex. Our research centres on using molecular tools to test among alternative mechanisms of developmental control tied to hormone titres, receptors and their timing in the life cycle. First, we synthesize detail about predator-induced defenses and the physiological regulation of arthropod somatic growth and morphology, leading to a clear prediction that morphological defences are regulated by juvenile hormone and life-history plasticity by ecdysone and juvenile hormone. We then show how a small network of genes can differentiate phenotype expression between the two primary developmental control pathways in arthropods: juvenoid and ecdysteroid hormone signalling. Then, by applying an experimental gradient of predation risk, we show dose-dependent gene expression linking predator-induced plasticity to the juvenoid hormone pathway. Our data support three conclusions: (1) the juvenoid signalling pathway regulates predator-induced phenotypic plasticity; (2) the hormone titre (ligand), rather than receptor, regulates predator-induced developmental plasticity; (3) evolution has favoured the harnessing of a major, highly conserved endocrine pathway in arthropod development to regulate the response to cues about changing environments (risk) from another organism (predator).