Insect herbivory and plant adaptation in an early successional community*

To address the role of insect herbivores in adaptation of plant populations and the persistence of selection through succession, we manipulated herbivory in a long‐term field experiment. We suppressed insects in half of 16 plots over nine years and examined the genotypic structure and chemical defense of common dandelion (Taraxacum officinale), a naturally colonizing perennial apomictic plant. Insect suppression doubled dandelion abundance in the first few years, but had negligible effects thereafter. Using microsatellite DNA markers, we genotyped >2500 plants and demonstrate that insect suppression altered the genotypic composition of plots in both sampling years. Phenotypic and genotypic estimates of defensive terpenes and phenolics from the field plots allowed us to infer phenotypic plasticity and the response of dandelion populations to insect‐mediated natural selection. The effects of insect suppression on plant chemistry were, indeed, driven both by plasticity and plant genotypic identity. In particular, di‐phenolic inositol esters were more abundant in plots exposed to herbivory (due to the genotypic composition of the plots) and were also induced in response to herbivory. This field experiment thus demonstrates evolutionary sorting of plant genotypes in response to insect herbivores that was in same direction as the plastic defensive response within genotypes.     

Drift versus selection as drivers of phenotypic divergence at small spatial scales: The case of Belgjarskógur threespine stickleback

Divergence in phenotypic traits is facilitated by a combination of natural selection, phenotypic plasticity, gene flow, and genetic drift, whereby the role of drift is expected to be particularly important in small and isolated populations. Separating the components of phenotypic divergence is notoriously difficult, particularly for multivariate phenotypes. Here, we assessed phenotypic divergence of threespine stickleback (Gasterosteus aculeatus) across 19 semi‐interconnected ponds within a small geographic region (~7.5 km²) using comparisons of multivariate phenotypic divergence (PST), neutral genetic (FST), and environmental (EST) variation. We found phenotypic divergence across the ponds in a suite of functionally relevant phenotypic traits, including feeding, defense, and swimming traits, and body shape (geometric morphometric). Comparisons of PSTs with FSTs suggest that phenotypic divergence is predominantly driven by neutral processes or stabilizing selection, whereas phenotypic divergence in defensive traits is in accordance with divergent selection. Comparisons of population pairwise PSTs with ESTs suggest that phenotypic divergence in swimming traits is correlated with prey availability, whereas there were no clear associations between phenotypic divergence and environmental difference in the other phenotypic groups. Overall, our results suggest that phenotypic divergence of these small populations at small geographic scales is largely driven by neutral processes (gene flow, drift), although environmental determinants (natural selection or phenotypic plasticity) may play a role.     

Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow

Divergent natural selection, adaptive divergence and gene flow may interact in a number of ways. Recent studies have focused on the balance between selection and gene flow in natural populations, and empirical work has shown that gene flow can constrain adaptive divergence, and that divergent selection can constrain gene flow. A caveat is that phenotypic diversification may be under the direct influence of environmental factors (i.e. it may be due to phenotypic plasticity), in addition to partial genetic influence. In this case, phenotypic divergence may occur between populations despite high gene flow that imposes a constraint on genetic divergence. Plasticity may dampen the effects of natural selection by allowing individuals to rapidly adapt phenotypically to new conditions, thus slowing adaptive genetic divergence. On the other hand, plasticity may promote future adaptive divergence by allowing populations to persist in novel environments. Plasticity may promote gene flow between selective regimes by allowing dispersers to adapt to alternate conditions, or high gene flow may result in the selection for increased plasticity. Here I expand frameworks for understanding relationships among selection, adaptation and gene flow to include the effects of phenotypic plasticity in natural populations, and highlight its importance in evolutionary diversification.     

克隆植物的表型可塑性与等级选择

表型可塑性是指生物个体生长发育过程中遭受不同环境条件作用时产生不同表型的能力。进化的发生有赖于自然选择对种群遗传可变性产生的效力以及各基因型的表型可塑性。有足够的证据说明表型可塑性的可遗传性,它实际上是进化改变的一个成分。一般通过优化模型、数量遗传模型和配子模型来研究表型可塑性的进化。植物的构型是相对固定的,并未完全抑制表型可塑性。克隆植物因其双构件性而具有更广泛的、具有重要生态适应意义的表型可塑性。构件性使克隆植物具有以分株为基本单位的等级结构,从而使克隆植物的表型选择也具有等级性。构件等级一般包含基株、克隆片段或分株系统以及分株3个典型水平。目前认为克隆植物的自然选择有两种模式,分别以等级选择模型和基因型选择模型表征。等级选择模型认为:不同的等级水平同时也是表型选择水平,环境对各水平具有作用,各水平之间也有相互作用,多重表型选择水平的净效应最终通过繁殖水平——分株传递到随后的世代中。基因型选择模型指出:克隆生长引起分株的遗传变异,并通过基株内分株间以及基株间的非随机交配引起种子库等位基因频率的改变,产生微进化。这两种选择模式均突出强调了分株水平在自然选择过程中的变异性以及在进化中的重要性,强调了克隆生长和种子繁殖对基株适合度的贡献。基因型选择模型包含等级选择模型的观点,是对等级选择模型的重要补充。克隆植物的表型可塑性表现在3个典型等级层次上,由于各层次对自然选择压力具有不同的反应,其表型变异程度一般表现出“分株层次>分株片段层次>基株层次”的等级性反应模式。很多证据表明,在构件有机体中构件具有最大的表型可塑性,植物的表型可塑性实际上是构件而非整个遗传个体的反应。这说明克隆植物的等级反应模式可能具有普适性。如果该反应模式同时还是构件等级中不同“个体”适应性可塑性反应的模式,那么可以预测:1)在克隆植物中,分株层次受到的自然选择强度也最大,并首先发生适应性可塑性变化,最终引起克隆植物微进化;2)由于较弱的有性繁殖能力,克隆植物在进化过程中的保守性可能大于非克隆植物。克隆植物等级反应模式的普适性亟待验证。     

Phenotypic convergence along a gradient of predation risk

A long-standing question in ecology is whether phenotypic plasticity, rather than selection per se, is responsible for phenotypic variation among populations. Plasticity can increase or decrease variation, but most previous studies have been limited to single populations, single traits and a small number of environments assessed using univariate reaction norms. Here, examining two genetically distinct populations of Daphnia pulex with different predation histories, we quantified predator-induced plasticity among 11 traits along a fine-scale gradient of predation risk by a predator (Chaoborus) common to both populations. We test the hypothesis that plasticity can be responsible for convergence in phenotypes among different populations by experimentally characterizing multivariate reaction norms with phenotypic trajectory analysis (PTA). Univariate analyses showed that all genotypes increased age and size at maturity, and invested in defensive spikes (neckteeth), but failed to quantitatively describe whole-organism response. In contrast, PTA quantified and qualified the phenotypic strategy the organism mobilized against the selection pressure. We demonstrate, at the whole-organism level, that the two populations occupy different areas of phenotypic space in the absence of predation but converge in phenotypic space as predation threat increases.     

Evolutionary stasis despite selection on a heritable trait in an invasive zooplankton

Invasive species are one of the greatest threats to ecosystems, and there is evidence that evolution plays an important role in the success or failure of invasions. Yet, few studies have measured natural selection and evolutionary responses to selection in invasive species, particularly invasive animals. We quantified the strength of natural selection on the defensive morphology (distal spine) of an invasive zooplankton, Bythotrephes longimanus, in Lake Michigan across multiple months during three growing seasons. We used multiple lines of evidence, including historic and contemporary wild‐captured individuals and palaeoecology of retrieved spines, to assess phenotypic change in distal spine length since invasion. We found evidence of temporally variable selection, with selection for decreased distal spine length early in the growing season and selection for increased distal spine length later in the season. This trend in natural selection is consistent with seasonal changes in the relative strength of non‐gape‐limited and gape‐limited fish predation. Yet, despite net selection for increased distal spine length and a known genetic basis for distal spine length, we observed little evidence of an evolutionary response to selection. Multiple factors likely limit an evolutionary response to selection, including genetic correlations, trade‐offs between components of fitness, and phenotypic plasticity.     

The consequences of phenotypic plasticity for ecological speciation

We use an individual-based numerical simulation to study the effects of phenotypic plasticity on ecological speciation. We find that adaptive plasticity evolves readily in the presence of dispersal between populations from different ecological environments. This plasticity promotes the colonization of new environments but reduces genetic divergence between them. We also find that the evolution of plasticity can either enhance or degrade the potential for divergent selection to form reproductive barriers. Of particular importance here is the timing of plasticity in relation to the timing of dispersal. If plasticity is expressed after dispersal, reproductive barriers are generally weaker because plasticity allows migrants to be better suited for their new environment. If plasticity is expressed before dispersal, reproductive barriers are either unaffected or enhanced. Among the potential reproductive barriers we considered, natural selection against migrants was the most important, primarily because it was the earliest-acting barrier. Accordingly, plasticity had a much greater effect on natural selection against migrants than on sexual selection against migrants or on natural and sexual selection against hybrids. In general, phenotypic plasticity can strongly alter the process of ecological speciation and should be considered when studying the evolution of reproductive barriers.     

Evolution of phenotypic plasticity: Genetic differentiation and additive genetic variation for induced plant defence in wild arugula Eruca sativa

Phenotypic plasticity is the primary mechanism of organismal resilience to abiotic and biotic stress, and genetic differentiation in plasticity can evolve if stresses differ among populations. Inducible defence is a common form of adaptive phenotypic plasticity, and long‐standing theory predicts that its evolution is shaped by costs of the defensive traits, costs of plasticity and a trade‐off in allocation to constitutive versus induced traits. We used a common garden to study the evolution of defence in two native populations of wild arugula Eruca sativa (Brassicaceae) from contrasting desert and Mediterranean habitats that differ in attack by caterpillars and aphids. We report genetic differentiation and additive genetic variance for phenology, growth and three defensive traits (toxic glucosinolates, anti‐nutritive protease inhibitors and physical trichome barriers) as well their inducibility in response to the plant hormone jasmonic acid. The two populations were strongly differentiated for plasticity in nearly all traits. There was little evidence for costs of defence or plasticity, but constitutive and induced traits showed a consistent additive genetic trade‐off within each population for the three defensive traits. We conclude that these populations have evolutionarily diverged in inducible defence and retain ample potential for the future evolution of phenotypic plasticity in defence.     

Host selection by the pine processionary moth enhances larval performance: An experiment

The development of a phytophagous insect depends on the nutritional characteristics of plants on which it feeds. Offspring from different females, however, may vary in their ability to develop in different host species and therefore females should place their eggs on host plants that result in the highest performance for the insect offspring. Causes underlying the predicted relationships between host selection and offspring performance may be: (1) a genetic association between larval ability to exploit particular hosts and the female insect's host preference; and (2) phenotypic plasticity of larvae that may be due to (a) maternal effects (e.g. differential investment in eggs) or (b) diet. In this work, we analyse the performance (i.e. hatching success and larval size and mortality) of the pine processionary (Thaumetopoea pityocampa) caterpillar developing in Aleppo (Pinus halepensis) or maritime (Pinus pinaster) pines. Larvae of this moth species do not move from the individual pine selected by the mother for oviposition. By means of cross-fostering experiments of eggs batches and silk nests of larvae between these two pine species, we explored whether phenotypic plasticity of offspring traits or genetic correlations between mother and offspring traits account for variation in developmental characteristics of caterpillars. Our results showed that females preferentially selected Aleppo pine for oviposition. Moreover, the offspring had the highest probability of survival and reached a larger body size in this pine species independently of whether or not batches were experimentally cross-fostered. Notably, the interaction between identity of donor and receiver pine species of larvae nests explained a significant proportion of variance of larval size and mortality, suggesting a role of diet-induced phenotypic plasticity of the hatchlings. These results suggest that both female selection of the more appropriate pine species and phenotypic plasticity of larva explain the performance of pine processionary caterpillars.     

Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail

Temporal and spatial patterns of phenotypic variation have traditionally been thought to reflect genetic differentiation produced by natural selection. Recently, however, there has been growing interest in how natural selection may shape the genetics of phenotypic plasticity to produce patterns of geographic variation and phenotypic evolution. Because the covariance between genetic and environmental influences can modulate the expression of phenotypic variation, a complete understanding of geographic variation requires determining whether these influences covary in the same (cogradient variation) or in opposing (countergradient variation) directions. We focus on marine snails from rocky intertidal shores as an ideal system to explore how genetic and plastic influences contribute to geographic and historical patterns of phenotypic variation. Phenotypic plasticity in response to predator cues, wave action, and water temperature appear to exert a strong influence on small and large-scale morphological variation in marine snails. In particular, plasticity in snail shell thickness: (i) may contribute to phenotypic evolution, (ii) appears to have evolved across small and large spatial scales, and (iii) may be driven by life history trade-offs tied to architectural constraints imposed by the shell. The plasticity exhibited by these snails represents an important adaptive strategy to the pronounced heterogeneity of the intertidal zone and undoubtedly has played a key role in their evolution.     

How stabilizing selection and nongenetic inheritance combine to shape the evolution of phenotypic plasticity

Relatively little is known about whether and how nongenetic inheritance interacts with selection to impact the evolution of phenotypic plasticity. Here, we empirically evaluated how stabilizing selection and a common form of nongenetic inheritance—maternal environmental effects—jointly influence the evolution of phenotypic plasticity in natural populations of spadefoot toads. We compared populations that previous fieldwork has shown to have evolved conspicuous plasticity in resource‐use phenotypes (“resource polyphenism”) with those that, owing to stabilizing selection favouring a narrower range of such phenotypes, appear to have lost this plasticity. We show that: (a) this apparent loss of plasticity in nature reflects a condition‐dependent maternal effect and not a genetic loss of plasticity, that is “genetic assimilation,” and (b) this plasticity is not costly. By shielding noncostly plasticity from selection, nongenetic inheritance generally, and maternal effects specifically, can preclude genetic assimilation from occurring and consequently impede adaptive (genetic) evolution.     

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.     

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.     

Analyzing reaction norm variation in the field vs. greenhouse: Comparing studies of plasticity and its adaptive value in two species of Erodium

Despite a wide range of experiments characterizing patterns of selection on phenotypic plasticity in controlled environments there has been virtually no research assessing the extent to which these results reflect selection on plasticity expressed in natural populations. To test how well the patterns observed in controlled experiments match the patterns in field populations, we present two case studies in which we characterized the fitness consequences of plasticity both under controlled lath house conditions and in the field. We quantified selection on plasticity in response to soil nutrient variation in two annual plant species, Erodium cicutarium and Erodium brachycarpum. For both species, families collected from the same source populations were used in both field and lath house experiments. We ask whether the qualitative results obtained from field and controlled environment experiments are equivalent. In two cases we observed selection on the expression of plasticity by E. brachycarpum in the field while controlled environment experiments indicated that plasticity was selectively neutral. In three other cases we observed differences in the pattern of plasticity expressed in the controlled environment experiment relative to the field resulting in conflicting results regarding the form of trait expression favored by selection. Based on these results, we argue that the extent to which results from controlled environments can be accurately extrapolated to naturally occurring populations depends on whether treatments imposed in a controlled environment accurately mimic environmental variation in the field and induce plasticity in traits of interest. Ideally any controlled environment experiment characterizing plasticity would be paired with field survey data of environmental and phenotypic variation within naturally occurring populations.     

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.     

MEASURING NATURAL SELECTION ON PHENOTYPIC PLASTICITY

To understand natural selection we need to integrate its measure across environments. We present a method for measuring phenotypic selection that combines the potential for both environmental variation and phenotypic plasticity. The method uses path analysis and a measure of selection that is analogous to selection on breeding values. For individuals growing in alternative environments, paths are created that represent potential changes in the environment. The probabilities for these changes are then multiplied by the path coefficients to calculate selection coefficients. Selection on plasticity is measured as the difference in selection within each environment. We illustrate these methods using data on selection in an experimental population of Arabidopsis thaliana. Individuals from 36 families were grown in one of four environments, a factorial combination of shaded/open and early/late shading. For final height of the inflorescence, there was positive selection in both the open and shaded environments and negative selection on plasticity of height. For bolting time, there was also positive selection in both environments, but no selection on plasticity. We show how to use this information to examine how selection would change with changes in environmental frequencies and their transition probabilities. These methods can be expanded to encompass continuous traits and continuous environments as well as other complexities of natural selection.     

Developmental plasticity and the origin of novel forms: unveiling cryptic genetic variation via "use and disuse"

Natural selection eliminates phenotypic variation from populations, generation after generation-an observation that haunted Darwin. So, how does new phenotypic variation arise, and is it always random with respect to fitness? Repeated behavioral responses to a novel environment-particularly those that are learned-are typically advantageous. If those behaviors yield more extreme or novel morphological variants via developmental plasticity, then previously cryptic genetic variation may be exposed to natural selection. Significantly, because the mean phenotypic effect of "use and disuse" is also typically favorable, previously cryptic genetic variation can be transformed into phenotypic variation that is both visible to selection and biased in an adaptive direction. Therefore, use-induced developmental plasticity in a very real sense "creates" new phenotypic variation that is nonrandom with respect to fitness, in contrast to the random phenotypic effects of mutation, recombination, and "direct effects" of environment (stress, nutrition). I offer here (a) a brief review of the immense literature on the effects of "use and disuse" on morphology, (b) a simple yet general model illustrating how cryptic genetic variation may be exposed to selection by developmentally plastic responses that alter trait performance in response to "use and disuse," and (c) a more detailed model of a positive feedback loop between learning (handed behavior) and morphological plasticity (use-induced morphological asymmetry) that may rapidly generate novel phenotypic variation and facilitate the evolution of conspicuous morphological asymmetries. Evidence from several sources suggests that handed behaviors played an important role both in the origin of novel forms (asymmetries) and in their subsequent evolution.     

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.     

Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis

Plants possess a remarkable capacity to alter their phenotype in response to the highly heterogeneous light conditions they commonly encounter in natural environments. In the present study with the weedy annual plant Sinapis arvensis, we (a) tested for the adaptive value of phenotypic plasticity in morphological and life history traits in response to low light and (b) explored possible fitness costs of plasticity. Replicates of 31 half-sib families were grown individually in the greenhouse under full light and under low light (40% of ambient) imposed by neutral shade cloth. Low light resulted in a large increase in hypocotyl length and specific leaf area (SLA), a reduction in juvenile biomass and a delayed onset of flowering. Phenotypic selection analysis within each light environment revealed that selection favoured large SLA under low light, but not under high light, suggesting that the observed increase in SLA was adaptive. In contrast, plasticity in the other traits measured was maladaptive (i.e. in the opposite direction to that favoured by selection in the low light environment). We detected significant additive genetic variance in plasticity in most phenotypic traits and in fitness (number of seeds). Using genotypic selection gradient analysis, we found that families with high plasticity in SLA had a lower fitness than families with low plasticity, when the effect of SLA on fitness was statistically kept constant. This indicates that plasticity in SLA incurred a direct fitness cost. However, a cost of plasticity was only expressed under low light, but not under high light. Thus, models on the evolution of phenotypic plasticity will need to incorporate plasticity costs that vary in magnitude depending on environmental conditions.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.