Phenotypic plasticity to light intensity in Arabidopsis thaliana: invariance of reaction norms and phenotypic integration

Phenotypic plasticity (the pattern of response of organisms to changes in environmental conditions) and phenotypic integration (the pattern of character correlations) are important components of our understanding of the evolution of complex phenotypes. Most studies published so far in this area have been conducted within populations with the express aim of predicting future response to evolutionary forces. However, among-population differentiation for plasticity and trait correlations are important indicators of recent past events that have shaped the currently observable phenotypes. We investigated variation in the reaction norms of several traits in a large number of accessions of Arabidopsis thaliana exposed to different levels of light quantity as well as the environmental lability of the corresponding across-population character variance–covariance matrix. Our results show that there is an astounding degree of inter-population variation for character means and very little variation for plasticity, in agreement with the idea that A. thaliana is a light-specialist often occurring in open, disturbed habitats. However, this plant also shows patterns of plasticity that are predicted to be adaptive based on functional ecological considerations, such as an increase in either specific leaf area or leaf number (but not both) under low light. We also demonstrate that the set of character correlations in A. thaliana is extremely stable to changes in light availability, contrary to previous findings in the same species when different environmental factors were considered. Several processes that might have been responsible for the observed patterns are discussed as a prelude to follow-up research on these problems.     

A modular concept of phenotypic plasticity in plants

Based on empirical evidence from the literature we propose that, in nature, phenotypic plasticity in plants is usually expressed at a subindividual level. While reaction norms (i.e. the type and the degree of plant responses to environmental variation) are a property of genotypes, they are expressed at the level of modular subunits in most plants. We thus contend that phenotypic plasticity is not a whole-plant response, but a property of individual meristems, leaves, branches and roots, triggered by local environmental conditions. Communication and behavioural integration of interconnected modules can change the local responses in different ways: it may enhance or diminish local plastic effects, thereby increasing or decreasing the differences between integrated modules exposed to different conditions. Modular integration can also induce qualitatively different responses, which are not expressed if all modules experience the same conditions. We propose that the response of a plant to its environment is the sum of all modular responses to their local conditions plus all interaction effects that are due to integration. The local response rules to environmental variation, and the modular interaction rules may be seen as evolving traits targeted by natural selection. Following this notion, whole-plant reaction norms are an integrative by-product of modular plasticity, which has far-reaching methodological, ecological and evolutionary implications.     

Phenotypic plasticity and morphological integration in a marine modular invertebrate

Background  

Colonial invertebrates such as corals exhibit nested levels of modularity, imposing a challenge to the depiction of their morphological evolution. Comparisons among diverse Caribbean gorgonian corals suggest decoupling of evolution at the polyp vs. branch/internode levels. Thus, evolutionary change in polyp form or size (the colonial module sensu stricto) does not imply a change in colony form (constructed of modular branches and other emergent features). This study examined the patterns of morphological integration at the intraspecific level. Pseudopterogorgia bipinnata (Verrill) (Octocorallia: Gorgoniidae) is a Caribbean shallow water gorgonian that can colonize most reef habitats (shallow/exposed vs. deep/protected; 1–45 m) and shows great morphological variation.     

Constraints on the evolution of adaptive phenotypic plasticity in plants

The high potential fitness benefit of phenotypic plasticity tempts us to expect phenotypic plasticity as a frequent adaptation to environmental heterogeneity. Examples of proven adaptive plasticity in plants, however, are scarce and most plastic responses actually may be 'passive' rather than adaptive. This suggests that frequently requirements for the evolution of adaptive plasticity are not met or that such evolution is impeded by constraints. Here we outline requirements and potential constraints for the evolution of adaptive phenotypic plasticity, identify open questions, and propose new research approaches. Important open questions concern the genetic background of plasticity, genetic variation in plasticity, selection for plasticity in natural habitats, and the nature and occurrence of costs and limits of plasticity. Especially promising tools to address these questions are selection gradient analysis, meta-analysis of studies on genotype-by-environment interactions, QTL analysis, cDNA-microarray scanning and quantitative PCR to quantify gene expression, and two-dimensional gel electrophoresis to quantify protein expression. Studying plasticity along the pathway from gene expression to the phenotype and its relationship with fitness will help us to better understand why adaptive plasticity is not more universal, and to more realistically predict the evolution of plastic responses to environmental change.     

Long-term in vitro culture affects phenotypic plasticity of Neoregelia johannis plants

Plant Cell, Tissue and Organ Culture (PCTOC) - We carried out immunoassay of plant hormones [indoleacetic acid (IAA), cytokinins and abscisic acid (ABA)] in the extracts from explants...     

Phenotypic plasticity in Phlox

Summary Three 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.     

Differences in phenotypic plasticity between plants from dimorphic seeds of Cakile edentula

The composition, structure and dendroecology of a 320-year-old Pinus rigida rock outcrop community was studied in the Shawangunk Mountains of southeastern New York. This represents one of the oldest known examples of this forest type and it is located on one of the most extreme sites in the northeastern United States. P. rigida represented 88% of all sampled trees, which typically grew on individual soil islands with soil depths of 8–35 cm surrounded by exposed bedrock. The forest was uneven-aged and P. rigida exhibited continuous recruitment into the tree size classes since the late 1600s, suggesting that it represents a physiographic climax for this species. However, a limited amount of Nyssa sylvatica and Quercus prinus recruitment started after 1830. Peak recruitment of P. rigida trees in 1720–1760 and 1860–1890 coincided with parabolic-shaped releases in their radial growth, possibly in response to disturbances. Tree ring growth was typically <0.4 mm/year since the 1850s and <0.3 mm/year during a prolonged and severe drought in the 1960s. However, large increases in precipitation and temperature from 1970 to 1993 were correlated with a dramatic post-drought growth response producing the highest ring width index values throughout the life of 260 to 280-year-old trees. Thus, we attribute certain moderate growth releases (>50%) lasting 10–15 years to climate, rather than disturbance. Tree growth and recruitment at the study site were influenced by a complex interaction of climate, soil and disturbance factors. Coupling of species recruitment, tree ring and climatic data in this study provided an improved technique for understanding forest growth and dynamics.     

Phenotypic plasticity and specialization in clonal versus non-clonal plants: A data synthesis

Reproductive strategies can be associated with ecological specialization and generalization. Clonal plants produce lineages adapted to the maternal habitat that can lead to specialization. However, clonal plants frequently display high phenotypic plasticity (e.g. clonal foraging for resources), factors linked to ecological generalization. Alternately, sexual reproduction can be associated with generalization via increasing genetic variation or specialization through rapid adaptive evolution. Moreover, specializing to high or low quality habitats can determine how phenotypic plasticity is expressed in plants. The specialization hypothesis predicts that specialization to good environments results in high performance trait plasticity and specialization to bad environments results in low performance trait plasticity. The interplay between reproductive strategies, phenotypic plasticity, and ecological specialization is important for understanding how plants adapt to variable environments. However, we currently have a poor understanding of these relationships. In this study, we addressed following questions: 1) Is there a relationship between phenotypic plasticity, specialization, and reproductive strategies in plants? 2) Do good habitat specialists express greater performance trait plasticity than bad habitat specialists? We searched the literature for studies examining plasticity for performance traits and functional traits in clonal and non-clonal plant species from different habitat types. We found that non-clonal (obligate sexual) plants expressed greater performance trait plasticity and functional trait plasticity than clonal plants. That is, non-clonal plants exhibited a specialist strategy where they perform well only in a limited range of habitats. Clonal plants expressed less performance loss across habitats and a more generalist strategy. In addition, specialization to good habitats did not result in greater performance trait plasticity. This result was contrary to the predictions of the specialization hypothesis. Overall, reproductive strategies are associated with ecological specialization or generalization through phenotypic plasticity. While specialization is common in plant populations, the evolution of specialization does not control the nature of phenotypic plasticity as predicted under the specialization hypothesis.     

Phenotypic plasticity in the developmental integration of morphological trade-offs and secondary sexual trait compensation

Trait exaggeration through sexual selection will tale place alongside other changes in phenotype. Exaggerated morphology might be compensated by parallel changes in traits that support, enhance or facilitate exaggeration: 'secondary sexual trait compensation' (SSTC). Alternatively, exaggeration might be realized at the expense of other traits through morphological trade-offs. For the most part, SSTC has only been examined interspecifically. For these phenomena to be important intraspecifically, the sexual trait must be developmentally integrated with the compensatory or competing trait. We studied developmental integration in two species with different development: the holometabolous beetle Onthophagus taurus and the hemimetabolous earwig Forficula auricularia. Male-dimorphic variation in trait exaggeration was exploited to expose both trade-offs and SSTC. We found evidence for morphological trade-offs in O. taurus, but no F. auricularia, supporting the notion that trade-offs are more likely in closed developmetal systems. However, we found these trade-offs were not limited solely to traits growing close together. Developmental integration of structures involved in SSTC were detected in both species. The developmental integration of SSTC was phenotypically plastic, such that the compensation for relatively larger sexual traits was greater in the exasperated male morphs. Evidence of intraspecific SSTC demands studies of the selective, genetic and developmental architecture of phenotypic integration.     

Phenotypic plasticity in bacterial plasmids

Plasmid pB15 was previously shown to evolve increased horizontal (infectious) transfer at the expense of reduced vertical (intergenerational) transfer and vice versa, a key trade-off assumed in theories of parasite virulence. Whereas the models predict that susceptible host abundance should determine which mode of transfer is selectively favored, host density failed to mediate the trade-off in pB15. One possibility is that the plasmid's transfer deviates from the assumption that horizontal spread (conjugation) occurs in direct proportion to cell density. I tested this hypothesis using Escherichia coli/pB15 associations in laboratory serial culture. Contrary to most models of plasmid transfer kinetics, my data show that pB15 invades static (nonshaking) bacterial cultures only at intermediate densities. The results can be explained by phenotypic plasticity in traits governing plasmid transfer. As cells become more numerous, the plasmid's conjugative transfer unexpectedly declines, while the trade-off between transmission routes causes vertical transfer to increase. Thus, at intermediate densities the plasmid's horizontal transfer can offset selection against plasmid-bearing cells, but at high densities pB15 conjugates so poorly that it cannot invade. I discuss adaptive vs. nonadaptive causes for the phenotypic plasticity, as well as potential mechanisms that may lead to complex transfer dynamics of plasmids in liquid environments.     

Phenotypic plasticity and diversity in insects

Phenotypic plasticity in general and polyphenic development in particular are thought to play important roles in organismal diversification and evolutionary innovation. Focusing on the evolutionary developmental biology of insects, and specifically that of horned beetles, I explore the avenues by which phenotypic plasticity and polyphenic development have mediated the origins of novelty and diversity. Specifically, I argue that phenotypic plasticity generates novel targets for evolutionary processes to act on, as well as brings about trade-offs during development and evolution, thereby diversifying evolutionary trajectories available to natural populations. Lastly, I examine the notion that in those cases in which phenotypic plasticity is underlain by modularity in gene expression, it results in a fundamental trade-off between degree of plasticity and mutation accumulation. On one hand, this trade-off limits the extent of plasticity that can be accommodated by modularity of gene expression. On the other hand, it causes genes whose expression is specific to rare environments to accumulate greater variation within species, providing the opportunity for faster divergence and diversification between species, compared with genes expressed across environments. Phenotypic plasticity therefore contributes to organismal diversification on a variety of levels of biological organization, thereby facilitating the evolution of novel traits, new species and complex life cycles.     

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.     

Phenotypic plasticity and social environment

Summary When individual organisms can differ phenotypically in ways that do not depend on the existence of genotypic differences among the individuals, they are said to be phenotypically plastic. Enhanced individual reproductive success in physically variable and/or uncertain environments is the conventional explanation for evolution of genetically based phenotypic plasticity. But this conventional wisdom seems inadequate in view of theoretical models demonstrating that individual ability to change sex, reproductive strategy, or location can evolve by natural selection in a stable, saturated, physically uniform habitat. I generalize these results to include the case of phenotypic plasticity. My models show that phenotypic plasticity can be evolutionarily stable in physically unvarying habitats as a consequence of social interactions. This approach to phenotypic plasticity challenges the accepted view that plasticity of phenotypes is non-adaptive or an adaptation to physical factors alone, and that natural selection cannot normally affect the mode of maintenance of phenotypic variation. The models may also offer additional perspectives on the evolution of sexual reproduction.     

Phenotypic plasticity for life history traits in Drosophila melanogaster. I. Effect on phenotypic and environmental correlations

All 36 possible crosses among 6 homozygous lines of Drosophila melanogaster were tested for their phenotypic response in developmental time and dry weight at eclosion to variation in temperature and yeast concentration. This method was chosen because it allows one to produce the same heterozygous offspring repeatedly for testing under more conditions than could be handled at once. We estimated the effects of yeast concentration and temperature and their interaction on both the phenotypic and the environmental components of variation and covariation of the two traits. Development was slower at low temperatures and yeast concentrations, and dry weight and viability were lower at higher temperatures and lower yeast levels. Interactions of the two factors with the crosses and with each other indicated that there were genetic differences in plasticity and that the sensitivity of a trait to one factor depended on the level of the other. The covariation of the two traits was generally weak within an environment. Across environments, its sign depended on the factor that changed between the environments: positive for temperature, negative for yeast concentration. These findings can be explained in terms of an established growth model for Drosophila larvae. We conclude that for plastic traits with moderate or low heritability, the relationship between the phenotypic and genetic covariance matrices may be a complex function of the environmental factors that affect the traits. Some implications for the prediction of the evolution in fluctuating environments are outlined.