Hilary S. Callahan

Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana

In laboratory studies of Arabidopsis thaliana, plants shaded by neighboring vegetation (or subject to treatments mimicking shade) flower at a younger developmental stage, and sometimes earlier in time. We examined whether this shade avoidance response varies among and within natural populations of A. thaliana, and whether it corresponds to variable selection regimes at shaded and unshaded field sites, by conducting a two-year reciprocal transplant study and a parallel greenhouse study that manipulated the presence and timing of shade. In the field, shading had limited or inconsistent impacts on survivorship across several phases of the growing season. The date of bolting was earlier at the shadier site compared to the less shady site, but in the greenhouse there was no significant shade- induced plasticity for this trait. In both studies, we detected directional selection gradients favoring earlier bolting in shade, but gradients favoring earlier bolting were as strong in nonshaded conditions. The number of rosette leaves at bolting (i.e., the developmental stage of flowering) was significantly reduced by shade in both studies. However, there was either no directional selection on this trait, or selection to flower with more rather than fewer leaves. Despite the contrast in habitats, there was limited differentiation between populations for survivorship, reproductive fitness, size-related or flowering time traits, and no differ- entiation for trait plasticities. Some traits were variable among families within populations. A trade-off between age and developmental stage may limit the response to selection for flowering time, possibly explaining limited local adaptation. The adaptive significance of shade-induced flowering time plasticity remains equivocal. Future studies of the plasticity of flowering time in A. thaliana should investigate the effects of shading regimes together with other environmental variables on size- and timing-related traits.

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, Costs of Phenotypes, and Costs of Plasticity

Why are some traits constitutive and others inducible? The term costs often appears in work addressing this issue but may be ambiguously defined. This review distinguishes two conceptually distinct types of costs: phenotypic costs and plasticity costs. Phenotypic costs are assessed from patterns of covariation, typically between a focal trait and a separate trait relevant to fitness. Plasticity costs, separable from phenotypic costs, are gauged by comparing the fitness of genotypes with equivalent phenotypes within two environments but differing in plasticity and fitness. Subtleties associated with both types of costs are illustrated by a body of work addressing predator‐induced plasticity. Such subtleties, and potential interplay between the two types of costs, have also been addressed, often in studies involving genetic model organisms. In some instances, investigators have pinpointed the mechanistic basis of plasticity. In this vein, microbial work is especially illuminating and has three additional strengths. First, information about the machinery underlying plasticity—such as structural and regulatory genes, sensory proteins, and biochemical pathways—helps link population‐level studies with underlying physiological and genetic mechanisms. Second, microbial studies involve many generations, large populations, and replication. Finally, empirical estimation of key parameters (e.g., mutation rates) is tractable. Together, these allow for rigorous investigation of gene interactions, drift, mutation, and selection—all potential factors influencing the maintenance or loss of inducible traits along with phenotypic and plasticity costs. Messages emerging from microbial work can guide future efforts to understand the evolution of plastic traits in diverse organisms.

Evolutionary Change in Continuous Reaction Norms

Understanding the evolution of reaction norms remains a major challenge in ecology and evolution. Investigating evolutionary divergence in reaction norm shapes between populations and closely related species is one approach to providing insights. Here we use a meta-analytic approach to compare divergence in reaction norms of closely related species or populations of animals and plants across types of traits and environments. We quantified mean-standardized differences in overall trait means (Offset) and reaction norm shape (including both Slope and Curvature). These analyses revealed that differences in shape (Slope and Curvature together) were generally greater than differences in Offset. Additionally, differences in Curvature were generally greater than differences in Slope. The type of taxon contrast (species vs. population), trait, organism, and the type and novelty of environments all contributed to the best-fitting models, especially for Offset, Curvature, and the total differences (Total) between reaction norms. Congeneric species had greater differences in reaction norms than populations, and novel environmental conditions increased the differences in reaction norms between populations or species. These results show that evolutionary divergence of curvature is common and should be considered an important aspect of plasticity, together with slope. Biological details about traits and environments, including cryptic variation expressed in novel environmental conditions, may be critical to understanding how reaction norms evolve in novel and rapidly changing environments.

Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies

Root traits vary enormously among plant species but we have little understanding of how this variation affects their functioning. Of central interest is how root traits are related to plant resource acquisition strategies from soil. We examined root traits of 33 woody species from northeastern US forests that form two of the most common types of mutualisms with fungi, arbuscular mycorrhizas (AM) and ectomycorrhizas (EM). We examined root trait distribution with respect to plant phylogeny, quantifying the phylogenetic signal (K statistic) in fine root morphology and architecture, and used phylogenetically independent contrasts (PICs) to test whether taxa forming different mycorrhizal associations had different root traits. We found a pattern of species forming roots with thinner diameters as species diversified across time. Given moderate phylogenetic signals (K = 0.44–0.68), we used PICs to examine traits variation among taxa forming AM or EM, revealing that hosts of AM were associated with lower branching intensity (rPIC = −0.77) and thicker root diameter (rPIC = −0.41). Because EM evolved relatively more recently and intermittently across plant phylogenies, significant differences in root traits and colonization between plants forming AM and EM imply linkages between the evolution of these biotic interactions and root traits and suggest a history of selection pressures, with trade-offs for supporting different types of associations. Finally, across plant hosts of both EM and AM, species with thinner root diameters and longer specific root length (SRL) had less colonization (rPIC = 0.85, −0.87), suggesting constraints on colonization linked to the evolution of root morphology.

Using Artificial Selection to Understand Plastic Plant Phenotypes

Abstract The plasticity of any given trait, which has a genetic basis and which may or may not be adaptive, can intensify or attenuate evolved responses, and can itself evolve in response to selection depending on the scale of spatial or temporal heterogeneity. To investigate the complex function and evolution of plastic traits, an appealing yet challenging approach is assessing responses to artificial selection. Here, I review how artificial selection has been employed to explore four botanical research themes: (1) relationships between plastic and evolved responses to multiple stresses, (2) integration of cellular, leaf-level, and whole-plant responses to altered CO2 concentrations, (3) photomorphogenic and photoperiodic development, both mediated by phytochrome photoreceptors, and (4) the evolution of the pest-induced myrosinase-glucosinolate system in cruciferous plants. These diverse topics are unified not only because they have been studied using artificial selection experiments, but also because they have considered variability in multiple traits affected by multiple factors in the external environment. Limitations of such research include a dearth of long-term studies; a surprising but often logistically necessary omission of control or replicate lines; and numerous issues relating to assessing impacts of inbreeding and drift. In addition to discussing options for circumventing such limitations, I draw attention to strategies for integrating the results of artificial selection studies with progress in functional and evolutionary genomics.

Experimentally reduced root-microbe interactions reveal limited plasticity in functional root traits in Acer and Quercus.

BACKGROUND AND AIMS Interactions between roots and soil microbes are critical components of below-ground ecology. It is essential to quantify the magnitude of root trait variation both among and within species, including variation due to plasticity. In addition to contextualizing the magnitude of plasticity relative to differences between species, studies of plasticity can ascertain if plasticity is predictable and whether an environmental factor elicits changes in traits that are functionally advantageous. METHODS To compare functional traits and trait plasticities in fine root tissues with natural and reduced levels of colonization by microbial symbionts, trimmed and surface-sterilized root segments of 2-year-old Acer rubrum and Quercus rubra seedlings were manipulated. Segments were then replanted into satellite pots filled with control or heat-treated soil, both originally derived from a natural forest. Mycorrhizal colonization was near zero in roots grown in heat-treated soil; roots grown in control soil matched the higher colonization levels observed in unmanipulated root samples collected from field locations. KEY RESULTS Between-treatment comparisons revealed negligible plasticity for root diameter, branching intensity and nitrogen concentration across both species. Roots from treated soils had decreased tissue density (approx. 10-20 %) and increased specific root length (approx. 10-30 %). In contrast, species differences were significant and greater than treatment effects in traits other than tissue density. Interspecific trait differences were also significant in field samples, which generally resembled greenhouse samples. CONCLUSIONS The combination of experimental and field approaches was useful for contextualizing trait plasticity in comparison with inter- and intra-specific trait variation. Findings that root traits are largely species dependent, with the exception of root tissue density, are discussed in the context of current literature on root trait variation, interactions with symbionts and recent progress in standardization of methods for quantifying root traits.