Do plants and animals differ in phenotypic plasticity?

This paper compares the flexibility in the nexus between phenotype and genotype in plants and animals. These taxa although considered to be fundamentally different are found to be surprisingly similar in the mechanisms used to achieve plasticity. Although non-cognitive behaviour occurs in plants, its range is limited, while morphological and developmental plasticity also occur to a considerable extent in animals. Yet both plants and animals are subject to unique constraints and thus need to find unique solutions to functional problems. A true comparison between the plant and animal phenotype would be a comparison between plants and sessile photosynthesizing colonial invertebrates. Such comparisons are lacking. However, they would provide important insights into the adaptive significance of plasticity in these groups. It is also suggested that a comparison of inflexible traits in these groups would provide an understanding of the constraints, as well as the costs and benefits, of a plastic versus non-plastic phenotype in plants and animals.     

Genetic and phenotypic divergence in an island bird: isolation by distance,by colonization or by adaptation?

Discerning the relative roles of adaptive and nonadaptive processes in generating differences among populations and species, as well as how these processes interact, is a fundamental aim in biology. Both genetic and phenotypic divergence across populations can be the product of limited dispersal and gradual genetic drift across populations (isolation by distance), of colonization history and founder effects (isolation by colonization) or of adaptation to different environments preventing migration between populations (isolation by adaptation). Here, we attempt to differentiate between these processes using island populations of Berthelot's pipit (Anthus berthelotii), a passerine bird endemic to three Atlantic archipelagos. Using microsatellite markers and approximate Bayesian computation, we reveal that the northward colonization of this species ca. 8500 years ago resulted in genetic bottlenecks in the colonized archipelagos. We then show that high levels of genetic structure exist across archipelagos and that these are consistent with a pattern of isolation by colonization, but not with isolation by distance or adaptation. Finally, we show that substantial morphological divergence also exists and that this is strongly concordant with patterns of genetic structure and bottleneck history, but not with environmental differences or geographic distance. Overall, our data suggest that founder effects are responsible for both genetic and phenotypic changes across archipelagos. Our findings provide a rare example of how founder effects can persist over evolutionary timescales and suggest that they may play an important role in the early stages of speciation.     

Predator‐induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.     

Evolution of phenotypic plasticity: where are we going now?

The study of phenotypic plasticity has progressed significantly over the past few decades. We have moved from variation for plasticity being considered as a nuisance in evolutionary studies to it being the primary target of investigations that use an array of methods, including quantitative and molecular genetics, as well as of several approaches that model the evolution of plastic responses. Here, I consider some of the major aspects of research on phenotypic plasticity, assessing where progress has been made and where additional effort is required. I suggest that some areas of research, such the study of the quantitative genetic underpinning of plasticity, have been either settled in broad outline or superseded by new approaches and questions. Other issues, such as the costs of plasticity are currently at the forefront of research in this field, and are likely to be areas of major future development.     

Increasing melanism along a latitudinal gradient in a widespread amphibian: local adaptation,ontogenic or environmental plasticity?

Background  

The thermal benefits of melanism in ectothermic animals are widely recognized, but relatively little is known about population differentiation in the degree of melanism along thermal gradients, and the relative contributions of genetic vs. environmental components into the level of melanism expressed. We investigated variation in the degree of melanism in the common frog (Rana temporaria; an active heliotherm thermoregulator) by comparing the degree of melanism (i) among twelve populations spanning over 1500 km long latitudinal gradient across the Scandinavian Peninsula and (ii) between two populations from latitudinal extremes subjected to larval temperature treatments in a common garden experiment.     

Mahonia invasions in different habitats: local adaptation or general-purpose genotypes?

Rapid evolutionary adaptations and phenotypic plasticity have been suggested to be two important, but not mutually exclusive, mechanisms contributing to the spread of invasive species. Adaptive evolution in invasive plants has been shown to occur at large spatial scales to different climatic regions, but local adaptation at a smaller scale, e.g. to different habitats within a region, has rarely been studied. Therefore, we performed a case study on invasive Mahonia populations to investigate whether local adaptation may have contributed to their spread. We hypothesized that the invasion success of these populations is promoted by adaptive differentiation in response to local environmental conditions, in particular to the different soils in these habitats. To test this hypothesis, we carried out a reciprocal transplantation experiment in the field using seedlings from five Mahonia populations in Germany that are representative for the range of habitats invaded, and a greenhouse experiment that specifically compared the responses to the different soils of these habitats. We found no evidence for local adaptation of invasive Mahonia populations because seedlings from all populations responded similarly to different habitats and soils. In a second greenhouse experiment we examined genetic variation within populations, but seedlings from different maternal families did not vary in their responses to soil conditions. We therefore suggest that local adaptation of seedlings does not play a major role for the invasion success of Mahonia populations and that phenotypic plasticity, instead, could be an important trait in this stage of the life cycle.     

Why are most aquatic plants widely distributed? Dispersal,clonal growth and small-scale heterogeneity in a stressful environment

Non-marine aquatic vascular plants generally show broad distributional ranges. Climatic factors seem to have limited effects on their distributions, besides the determination of major disjunctions (tropical–temperate–subarctic). Dispersal should have been frequent enough to assure the quick colonisation of extensive areas following glacial retreat, but dispersal limitation is still apparent in areas separated by geographic barriers. Aquatic vascular plants also show limited taxonomic differentiation and low within-species genetic variation. Variation within populations is particularly low, but variation among populations seems to be relatively high, mainly due to the persistence of long-lived clones. Ecotypic differentiation is often related to factors that constrain clonal reproduction (salinity and ephemeral inundation). Inland aquatic habitats are heterogeneous environments, but this heterogeneity largely occurs at relatively small scales (within waterbodies and among neighbouring ones). They also represent a stressful environment for plants, characterised by low carbon availability, shaded conditions, sediment anoxia, mechanical damage by currents and waves, significant restrictions to sexual reproduction, and sometimes also osmotic stress and limited nutrient supply. I propose that the generality of broad distributions and low differentiation among the inland aquatic flora is best explained by a combination of: (1) selection for stress-tolerant taxa with broad tolerance ranges. (2) The selective advantages provided by clonal growth and multiplication, which increases plant tolerance to stress, genet survivorship and population viability. (3) Long-distance dispersal of sexual propagules and high local dispersal of asexual clones. (4) The generality of broad plastic responses, promoted by the combination of clonal growth, high local dispersal, small-scale spatial heterogeneity and temporal variability.     

Is local adaptation in Mimulus guttatus caused by trade‐offs at individual loci?

Local adaptation is considered to be the result of fitness trade‐offs for particular phenotypes across different habitats. However, it is unclear whether such phenotypic trade‐offs exist at the level of individual genetic loci. Local adaptation could arise from trade‐offs of alternative alleles at individual loci or by complementary sets of loci with different fitness effects of alleles in one habitat but selective neutrality in the alternative habitat. To evaluate the genome‐wide basis of local adaptation, we performed a field‐based quantitative trait locus (QTL) mapping experiment on recombinant inbred lines (RILs) created from coastal perennial and inland annual races of the yellow monkeyflower (Mimulus guttatus) grown reciprocally in native parental habitats. Overall, we detected 19 QTLs affecting one or more of 16 traits measured in two environments, most of small effect. We identified 15 additional QTL effects at two previously identified candidate QTLs [DIV ERGENCE (DIV)]. Significant QTL by environment interactions were detected at the DIV loci, which was largely attributable to genotypic differences at a single field site. We found no detectable evidence for trade‐offs for any one component of fitness, although DIV2 showed a trade‐off involving different fitness traits between sites, suggesting that local adaptation is largely controlled by non‐overlapping loci. This is surprising for an outcrosser, implying that reduced gene flow prevents the evolution of individuals adapted to multiple environments. We also determined that native genotypes were not uniformly adaptive, possibly reflecting fixed mutational load in one of the populations.     

How much do phenotypic plasticity and local genetic variation contribute to phenotypic divergences along environmental gradients in widespread invasive plants? A meta‐analysis

For introduced species that have spread across a wide distributional range, phenotypic plasticity (PLA) has often been proposed as an important contributor to invasion success, because it increases the survival rate during initial colonization. In contrast, local genetic variation (LOC) has also been proposed to be important, because it could allow invaders to evolve high performance in a new habitat. While evolutionary ecologists have long been interested in understanding genetic mechanisms that allow rapid colonization and spread of species, until recently experimental tests of these concepts have been limited. As a step towards generalization in our understanding of the importance of PLA and LOC, we review the current state of the literature on this topic using meta‐analysis. Here, we focused on three fundamental questions: 1) which strategy, PLA or LOC, better explains the phenotypic divergences during invader range expansion across different environmental gradients? 2) Which species characteristics correlate with the occurrence of these different phenomena? And 3) does the detection of PLA versus LOC depend on the trait studied? Using meta‐analysis we found that plasticity explained a higher proportion of phenotypic variation regardless of the environmental gradients studied or plant growth forms. PLA predominated in clonal, self‐compatible and perennial species, while LOC predominated in annual species. The patterns were trait‐dependent: LOC was significantly more important than PLA in phenology, while opposite patterns were found in fecundity and biomass allocation. The frequent simultaneous detection of PLA and genotypic variation in PLA among invasive populations suggested that PLA might benefit from LOC to some extent. Our results also indicate that the contribution of plasticity to the competitive advantages of invasive plants may be more informative than the level of plasticity itself. Synthesis For invasive plants that spread across a wide distributional range, understanding the mechanisms that allow rapid colonization and spread is crucial. Phenotypic plasticity (PLA) and local genetic variation (LOC) are both believed to play important roles in promoting range expansion. However, it is not clear which mechanism, PLA or LOC, contributes more to this process. According to our meta–analysis, PLA explained a higher proportion of adaptive phenotypic variation in most cases. Nevertheless, the predominance of an expansion mechanism depends on species characteristics and the trait studied. PLA may benefit from LOC to some extent. We suggest that the contribution of PLA to range expansion may better explain plant invasion success than the level of PLA itself.     

Re-orienting in space: do animals use global or local geometry strategies?

Here we compare whether birds encode surface geometry using principal axes, medial axes or local geometry. Birds were trained to locate hidden food in two geometrically identical corners of a rectangular arena and subsequently tested in an L-shaped arena. The chicks showed a primary local geometry strategy, and a secondary medial axes strategy, whereas the pigeons showed a medial axes strategy. Neither species showed behaviour supportive of the use of principal axes. This is, to our knowledge, the first study to directly examine these three current theories of geometric encoding.     

Experimental evolution of phenotypic plasticity: how predictive are cross-environment genetic correlations?

Genetic correlations are often predictive of correlated responses of one trait to selection on another trait. There are examples, however, in which genetic correlations are not predictive of correlated responses. We examine how well a cross-environment genetic correlation predicts correlated responses to selection and the evolution of phenotypic plasticity in the seed beetle Stator limbatus. This beetle exhibits adaptive plasticity in egg size by laying large eggs on a resistant host and small eggs on a high-quality host. From a half-sib analysis, the cross-environment genetic correlation estimate was large and positive (rA=0.99). However, an artificial-selection experiment on egg size found that the realized genetic correlations were positive but asymmetrical; that is, they depended on both the host on which selection was imposed and the direction of selection. The half-sib estimate poorly predicted the evolution of egg size plasticity; plasticity evolved when selection was imposed on one host but did not evolve when selection was imposed on the other host. We use a simple two-locus additive genetic model to explore the conditions that can generate the observed realized genetic correlation and the observed pattern of plasticity evolution. Our model and experimental results indicate that the ability of genetic correlations to predict correlated responses to selection depends on the underlying genetic architecture producing the genetic correlation.     

Differences in the onset of laying between island and mainland Mediterranean Blue Tits Parus caeruleus: phenotypic plasticity or genetic differences?

Blue tits Parus caeruleus breeding in deciduous or in evergreen woodlands on the mainland of Europe start to lay 3–4 weeks earlier than Blue Tits on the island of Corsica breeding in evergreen woodlands. A similar difference in average laying date between the two Blue Tit populations has been found in a relatively small sample of captive birds held in outdoor aviaries on the mainland. To provide data on the habitat contrast in Corsica for comparison with that on the mainland, a new study area was started in one of the few deciduous woodlands on Corsica. In addition, new data on laying dates of captive Blue Tits were gathered to increase the sample size of independent pairs in aviaries. This study shows that the habitat effect (deciduous ν evergreen woodland) on the average laying date of Blue Tits is relatively small in comparison with the geography effect (European mainland ν Corsica). The laying date differences between mainland and insular Blue Tits persisted whatever the type of habitat (deciduous, evergreen or outdoor aviaries on the mainland). The data support the hypothesis that the observed differences in the onset of laying between the mainland and insular Blue Tits were mainly influenced by genetic effects and relatively little by non-genetic maternal effects of by genotype—environment interactions.     

Extreme phenotypic variation in Cetraria aculeata (lichenized Ascomycota): adaptation or incidental modification?

Background and Aims

Phenotypic variability is a successful strategy in lichens for colonizing different habitats. Vagrancy has been reported as a specific adaptation for lichens living in steppe habitats around the world. Among the facultatively vagrant species, the cosmopolitan Cetraria aculeata apparently forms extremely modified vagrant thalli in steppe habitats of Central Spain. The aim of this study was to investigate whether these changes are phenotypic plasticity (a single genotype producing different phenotypes), by characterizing the anatomical and ultrastructural changes observed in vagrant morphs, and measuring differences in ecophysiological performance.

Methods

Specimens of vagrant and attached populations of C. aculeata were collected on the steppes of Central Spain. The fungal internal transcribed spacer (ITS), glyceraldehyde-3-phosphate dehydrogenase (GPD) and the large sub-unit of the mitochondrial ribosomal DNA (mtLSUm), and the algal ITS and actin were studied within a population genetics framework. Semi-thin and ultrathin sections were analysed by means of optical, scanning electron and transmission electron microscopy. Gas exchange and chlorophyll fluorescence were used to compare the physiological performance of both morphs.

Key Results and Conclusions

Vagrant and attached morphs share multilocus haplotypes which may indicate that they belong to the same species in spite of their completely different anatomy. However, differentiation tests suggested that vagrant specimens do not represent a random sub-set of the surrounding population. The morphological differences were related to anatomical and ultrastructural differences. Large intercalary growth rates of thalli after the loss of the basal–apical thallus polarity may be the cause of the increased growth shown by vagrant specimens. The anatomical and morphological changes lead to greater duration of ecophysiological activity in vagrant specimens. Although the anatomical and physiological changes could be chance effects, the genetic differentiation between vagrant and attached sub-populations and the higher biomass of the former show fitness effects and adaptation to dry environmental conditions in steppe habitats.     

Sex allocation in clonal plants: might clonal expansion enhance fitness gains through male function?

The returns on investment in sexual reproduction are described by fitness gain curves and the shapes of these curves affect, among other things, the evolutionary stability of reproductive systems. The available evidence indicates that gain curves for male function decelerate, corresponding to diminishing fitness returns on investment in pollen. In contrast, the gain curve for female function is thought to decelerate less strongly than it does for male function (e.g., if seed fertility is limited by more by resources than by mating opportunities). Here we suggest that when the shapes of the female and male gain curves differ, clonality alters the rates of return on investment via the two sex functions. In particular, we propose that clonal expansion might increase fitness gains through male function because the subdivision of reproductive effort among ramets allows each ramet to take advantage of the steepest parts of the male gain curve. We examined the interaction between clonal expansion and fitness gains using numerical analysis of a model of sex allocation in which we assumed that there is no mating interference among ramets. We found that clonal expansion led to substantial increases in fitness through male function, but to decreases in fitness through female function. Under intermediate investment in clonal growth, marginal fertility gains through the two sex functions did not intersect over a broad range of sex allocation patterns, suggesting that clonality could favor the evolution of separate sexes. Finally, we suggest an alternative explanation for the common observation of male-biased sex ratios in clonal dioecious plants. If male function fitness is maximized under higher rates of clonal expansion than for female function, greater frequencies of male ramets might reflect the outcome of fertility selection, rather than constraints on clonal expansion imposed by greater costs of reproduction for females.     

The genomics of local adaptation in trees: are we out of the woods yet?

There is substantial interest in uncovering the genetic basis of the traits underlying adaptive responses in tree species, as this information will ultimately aid conservation and industrial endeavors across populations, generations, and environments. Fundamentally, the characterization of such genetic bases is within the context of a genetic architecture, which describes the mutlidimensional relationship between genotype and phenotype through the identification of causative variants, their relative location within a genome, expression, pleiotropic effect, environmental influence, and degree of dominance, epistasis, and additivity. Here, we review theory related to polygenic local adaptation and contextualize these expectations with methods often used to uncover the genetic basis of traits important to tree conservation and industry. A broad literature survey suggests that most tree traits generally exhibit considerable heritability, that underlying quantitative genetic variation (Q_ST) is structured more so across populations than neutral expectations (F_ST) in 69% of comparisons across the literature, and that single-locus associations often exhibit small estimated per-locus effects. Together, these results suggest differential selection across populations often acts on tree phenotypes underlain by polygenic architectures consisting of numerous small to moderate effect loci. Using this synthesis, we highlight the limits of using solely single-locus approaches to describe underlying genetic architectures and close by addressing hurdles and promising alternatives towards such goals, remark upon the current state of tree genomics, and identify future directions for this field. Importantly, we argue, the success of future endeavors should not be predicated on the shortcomings of past studies and will instead be dependent upon the application of theory to empiricism, standardized reporting, centralized open-access databases, and continual input and review of the community’s research.     

Reproductive effort in clonal plants: constant allocation ratios among ramets?

Summary Armstrong (1982, 1983) predicted that all ramets within a clone should have the same ratio of biomass allocation to sexual reproduction versus vegetative growth. He presented data (1984) that he interpreted as showing that Solidago altissima ramets in a clone do have the predicted constant allocation ratio. Reanalysis of his methods shows that this conclusion was an artifact of his analysis. A simulation using random numbers and Armstrong's analysis showed the same pattern as his data. Data from S. altissima ramets of a single clone grown in a greenhouse experiment, using a different analysis, illustrated that the allocation ratios within a clone can be highly variable.     

The genomes and transposable elements in plants: are they friends or foes?

Transposable elements (TEs) are mobile genetic elements that are present in prokaryotes and eukaryotes. The ubiquity and abundance of these self-replicating entities, bereft of cellular function, had earned them the label of ‘genomic parasites’. However, the status of TEs has been revised, with ample genomic and biological evidence now portraying them as “genomic gold”. They are perceived as a major participant in the evolution of species. This review addresses the classification of TEs as well as their role and significance in the evolution of genomes, genetic diversity, gene regulation, and exaptation of contemporary species of the plant and animal kingdoms.     

Positive interactions by cushion plants in high mountains: fact or artifact?

Aims Positive interactions are defined as non-trophic interactions where at least one of the interacting species is benefited in terms of fitness and the other remains unaffected. Nevertheless, the bidirectional feedbacks between species may be positive, neutral or negative. Thus, if facilitated species induce negative effects on their 'nurses', the assumed definition of positive interactions could be reconsidered.Methods We assessed if ecological interactions between cushions of Azorella madreporica and their facilitated species are positive. Specifically, we tested if cover of facilitated species has any costs for cushion plants from an ecophysiological perspective, and if these costs increase with the amount of cover of facilitated species. In addition, through pathway analysis and correlations, we assessed if cover and richness of facilitated species have a direct and/or indirect effect on the fitness of cushion plants.Important findings We found that facilitated plant species induced a significant cost for their nurses (cushion plants), and this cost increases with cover of the facilitated species. Additionally, the facilitated species exert a strong direct negative effect on the cushion's fitness and a moderate indirect negative cost evident through the nutrient status and physiological performance of cushion plants. We thus contribute evidence that positive interactions between high mountain cushion plants of central Chile and their 'facilitated' species may be an artifact more than a fact, especially when bidirectional effects are considered; contrasting with the majority of studies that document only one side of the interaction.     

Overcompensation by plants: Herbivore optimization or red herring?

Summary The increased growth rates, higher total biomass, and increased seed production occasionally found in grazed or clipped plants are more accurately interpreted as the results of growth at one end of a spectrum of normal plant regrowth patterns, rather than as overcompensation, herbivore-stimulated growth, plantherbivore mutualisms, or herbivore enhanced fitness. Plants experience injury from a wide variety of sources besides herbivory, including fire, wind, freezing, heat, and trampling; rapid regrowth may have been selected for by any one of the many types of physical disturbance or extreme conditions that damage plant tissues, or by a combination of all of them. Rapid plant regrowth is more likely to have evolved as a strategy to reduce the negative impacts of all types of damage than as a strategy to increase fitness following herbivory above ungrazed levels. There is no evolutionary justification and little evidence to support the idea that plant-herbivore mutualisms are likely to evolve. Neither life history theory nor recent theoretical models provide plausible explanations for the benefits of herbivory.Several assumptions underlie all discussions of the benefits of herbivory: that plant species are able to evolve a strategy of depending on herbivores to increase their productivity and fitness; that herbivores do not preferentially regraze the overcompensating plants; that resources will be sufficient for regrowth; and that being larger is always better than being smaller. None of these assumptions is necessarily correct.