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.     

Toward a population genetic framework of developmental evolution: the costs,limits, and consequences of phenotypic plasticity

Adaptive phenotypic plasticity allows organisms to cope with environmental variability, and yet, despite its adaptive significance, phenotypic plasticity is neither ubiquitous nor infinite. In this review, we merge developmental and population genetic perspectives to explore costs and limits on the evolution of plasticity. Specifically, we focus on the role of modularity in developmental genetic networks as a mechanism underlying phenotypic plasticity, and apply to it lessons learned from population genetic theory on the interplay between relaxed selection and mutation accumulation. We argue that the environmental specificity of gene expression and the associated reduction in pleiotropic constraints drive a fundamental tradeoff between the range of plasticity that can be accommodated and mutation accumulation in alternative developmental networks. This tradeoff has broad implications for understanding the origin and maintenance of plasticity and may contribute to a better understanding of the role of plasticity in the origin, diversification, and loss of phenotypic diversity.     

植物表型可塑性研究进展

表型可塑性已成为生态进化发育生物学的核心概念,很大程度上由于植物可塑性研究的主要贡献,但人们仍远未完全了解表型可塑性的原因和结果。从整体角度理出表型可塑性研究发展的基本脉络,介绍研究内容、途径和简史,聚焦于几个主要方面的研究进展及发展方向。现代可塑性研究的兴盛始于关于可塑性的进化学重要性的一篇综述,从现象的描述、对其遗传基础和可塑性本身进化的讨论,发展到探索其背后的发育机制、植物生长与适应策略、生态学影响等。未来可塑性研究应在重新理解和评价表型可塑性及其适应性的基础上,更关注自然条件下环境因子和可塑响应的复杂性。表型可塑性的生态-进化学意义仍将是未来研究的重点。     

Early developmental plasticity and integrative responses in arctic charr (Salvelinus alpinus): effects of water velocity on body size and shape

Environmental conditions such as temperature and water velocity may induce changes among alternative developmental pathways, i.e. phenotypic responses, in vertebrates. However, the extent to which the environment induces developmental plasticity and integrated developmental responses during early ontogeny of fishes remains poorly documented. We analyzed the responses of newly hatched Arctic charr (Salvelinus alpinus) to four experimental water velocities during 100 days of development. To our knowledge, this work is the first to analyze developmental plasticity responses of body morphology to an experimental gradient of water velocities during early ontogeny of fish. Arctic charr body size and shape responses show first, that morphometric traits display significant differences between low and high water velocities, thus revealing directional changes in body traits. Secondly, trait variation allows the recognition of critical ontogenetic periods that are most responsive to environmental constraints (40-70 and 80-90 days) and exhibit different levels of developmental plasticity. This is supported by the observation of asynchronous timing of variation peaks among treatments. Third, morphological interaction of traits is developmentally plastic and time-dependent. We suggest that developmental responses of traits plasticity and interaction at critical ontogenetic periods are congruent with specific environmental conditions to maintain the functional integrity of the organism.     

Constraints on the evolution of phenotypic plasticity in the clonal plant Hydrocotyle vulgaris

The evolution of phenotypic plasticity of plant traits may be constrained by costs and limits. However, the precise constraints are still unclear for many traits under different ecological contexts. In a glasshouse experiment, we grew ramets of 12 genotypes of a clonal plant Hydrocotyle vulgaris under the control (full light and no flood), shade and flood conditions and tested the potential costs and limits of plasticity in 13 morphological and physiological traits in response to light availability and flood variation. In particular, we used multiple regression and correlation analyses to evaluate potential plasticity costs, developmental instability costs and developmental range limits of each trait. We detected significant costs of plasticity in specific petiole length and specific leaf area in response to shade under the full light condition and developmental range limits in specific internode length and intercellular CO₂ concentration in response to light availability variation. However, we did not observe significant costs or limits of plasticity in any of the 13 traits in response to flood variation. Our results suggest that the evolution of phenotypic plasticity in plant traits can be constrained by costs and limits, but such constraints may be infrequent and differ under different environmental contexts.     

Plasticity paves the way in an adaptive radiation

Phenotypic plasticity has been hypothesized to play a central role in the evolution of phenotypic diversity across species (West‐Eberhard 2003 ). Through ‘genetic assimilation’, phenotypes that are initially environmentally induced within species become genetically fixed over evolutionary time. While genetic assimilation has been shown to occur in both the laboratory and the field (Waddington 1953 ; Aubret & Shine 2009 ), it remains to be shown whether it can account for broad patterns of phenotypic diversity across entire adaptive radiations. Furthermore, our ignorance of the underlying molecular mechanisms has hampered our ability to incorporate phenotypic plasticity into models of evolutionary processes. In this issue of Molecular Ecology, Parsons et al. ( 2016 ) take a significant step in filling these conceptual gaps making use of cichlid fishes as a powerful study system. Cichlid jaw and skull morphology show adaptive, plastic changes in response to early dietary experiences (Fig. 1). In this research, Parsons et al. ( 2016 ) first show that the direction of phenotypic plasticity aligns with the major axis of phenotypic divergence across species. They then dissect the underlying genetic architecture of this plasticity, showing that it is specific to the developmental environment and implicating the patched locus in genetic assimilation (i.e. a reduction in the environmental sensitivity of that locus in the derived species).     

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

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

Biological evolution as an expression of body-plan potentialities.

A growing bulk of recent data from different fields as molecular biology, developmental biology, genetics, paleontology and phylogenetics shows that organisms play a more active role in their evolution than what postulated by the random variation-natural selection paradigm of the neo-Darwinian synthesis. Organisms show during development and morphogenesis autopoietic processes which are related to their body-plan potentialities. These potentialities are expressed through regulatory networks in which a plastic genome participates together with proteins and other substances in an epigenetic space. The epigenetic systems which arise from this interaction may be inherited and then assume a significant role in evolution becoming the source of new acquired characters. The acquisition of new traits through the epigenetic systems is influenced directly by environmental cues. If this process is coherent with the environmental demands it co-operates with natural selection in organism adaptation. An outstanding role in this context may be played by phenotypic plasticity if, as emerges in recent views, it may constitute a general basis for genetic assimilation processes.     

Developmental Plasticity: Developmental Conversion versus Phenotypic Modulation

The developmental mechanisms by which the environment may alterthe phenotype during development are reviewed. Developmentalplasticity may be of two forms: developmental conversion orphenotypic modulation. In developmental conversion, organismsuse specific environmental cues to activate alternative geneticprograms controlling development. These alternative programsmay either lead to alternative morphs, or may lead to the decisionto activate a developmental arrest. In phenotypic modulation,nonspecific phenotypic variation results from environmentalinfluences on rates or degrees of expression of the developmentalprogram, but the genetic programs controlling development arenot altered. Modulation, which is not necessarily adaptive,is probably the common form of environmentally induced phenotypicvariation in higher organisms, and adaptiveness of phenotypicplasticity therefore cannot be assumed unless specific geneticmechanisms can be demonstrated. The genetic mechanisms by whichdevelopmental plasticity may evolve are reviewed, and the relationshipbetween developmental plasticity and evolutionary plasticityare examined.     

Hominin homoiology: an assessment of the impact of phenotypic plasticity on phylogenetic analyses of humans and their fossil relatives

Homoiologies are phylogenetically misleading morphological similarities that are due to nongenetic factors. It has been claimed that homoiologies are common in the hominin skull, especially in regions affected by masticatory strain, and that their prevalence is one reason why reconstructing hominin phylogenetic relationships is difficult. To evaluate this "homoiology hypothesis," we performed analyses on a group of extant primates for which a robust molecular phylogeny is available--the hominoids. We compiled a data set from measurements that developmental considerations and experimental evidence suggest differ in their likelihood of exhibiting masticatory-strain-induced phenotypic plasticity. We then used the coefficient of variation and t-tests to evaluate the phenotypic plasticity of the measurements. We predicted that, if the hypothesis is correct, the measurements of skeletal features that do not remodel and therefore are unaffected by phenotypic plasticity should be less variable than the measurements of skeletal features that remodel and are subject to low-to-moderate strains, and that the latter should be less variable than the measurements of skeletal features that remodel and are subject to moderate-to-high strains. Subsequently, we performed phylogenetic analyses on character state data derived from the measurements and compared the resulting phylogenetic hypotheses to the consensus molecular phylogeny for the hominoids. We predicted that, if the hypothesis is correct, agreement between the phylogenies should be best for the non-phenotypically-plastic characters, intermediate for the low-to-moderate-strain characters, and worst for the moderate-to-high-strain characters. The results of the coefficient of variation/t-test analyses were consistent with the predictions of the hypothesis to the extent that the moderate-to-high-strain measurements exhibited significantly more variability than the non-phenotypically-plastic and low-to-moderate-strain measurements. In contrast, the results of the phylogenetic analyses were not those predicted. The phylogeny derived from the moderate-to-high-strain characters matched the molecular phylogeny better than those obtained using the non-phenotypically-plastic and low-to-moderate-strain characters. Thus, our study supports the suggestion that mechanical loading results in phenotypic plasticity in the hominin skull, but it does not support the notion that homoiologies have a significant negative impact on hominin phylogenetics.     

Rapid adaptation: a new dimension for evolutionary perspectives in ecology

Although the study of adaptation is central to biology, two types of adaptation are recognized in the biological field: physiological adaptation (accommodation or acclimation; an individual organism’s phenotype is adjusted to its environment) and evolutionary–biological adaptation (adaptation is shaped by natural selection acting on genetic variation). The history of the former concept dates to the late nineteenth and early twentieth centuries, and has more recently been systemized in the twenty-first century. Approaches to the understanding of phenotypic plasticity and learning behavior have only recently been developed, based on cellular–histological and behavioral–neurobiological techniques as well as traditional molecular biology. New developments of the former concepts in phenotypic plasticity are discussed in bacterial persistence, wing di-/polymorphism with transgenerational effects, polyphenism in social insects, and defense traits for predator avoidance, including molecular biology analyses. We also discuss new studies on the concept of genetic accommodation resulting in evolution of phenotypic plasticity through a transgenerational change in the reaction norm based on a threshold model. Learning behavior can also be understood as physiological phenotypic plasticity, associating with the brain–nervous system, and it drives the accelerated evolutionary change in behavioral response (the Baldwin effect) with memory stock. Furthermore, choice behaviors are widely seen in decision-making of animal foragers. Incorporating flexible phenotypic plasticity and learning behavior into modeling can drastically change dynamical behavior of the system. Unification of biological sciences will be facilitated and integrated, such as behavioral ecology and behavioral neurobiology in the area of learning, and evolutionary ecology and molecular developmental biology in the theme of phenotypic plasticity.     

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.     

Ecological constraints on the evolution of plasticity in plants

Signal detection and response are fundamental to all aspects of phenotypic plasticity. This paper proposes a novel mechanism that may act as a general limit to the evolution of plasticity, based on how selection on signal detection and response is likely to interact with gene flow in a spatially autocorrelated environment. The factors promoting the evolution of plasticity are reviewed, highlighting the crucial role of information acquisition and developmental lags, and of selection in spatially and temporally structured habitats. Classic studies of the evolution of plasticity include those on shade avoidance, on morphological plasticity in clonal plants, and on selection in spatially structured model populations. Comparative studies indicate that, among clonal plants, extensive plasticity in growth form is favored in patchy environments, as expected. However, among woody lineages from Madagascar, plasticity in photosynthetic pathway (CAM vs. C₃) appears to confer competitive success in areas of intermediate drought stress, rather than allowing individually plastic species to expand their ranges, as has often been argued. The extent of phenotypic plasticity cannot only determine species distributions, it can also affect the sign and magnitude of interactions between species. There appears to be some relationship between developmental plasticity and evolutionary lability: traits that show relatively few transitions within and among plant lineages (e.g., zygomorphy vs. actinomorphy, phyllotaxis, fleshy vs. capsular fruits) usually show no plasticity within individual plants; traits that show extensive plasticity within individuals or species (e.g., leaf size, flower number, plant height) generally also show extensive variation within and across lineages. Transaction and cybernetic costs, as well as long-lived leaves or roots, can limit the tempo of adaptive developmental responses, and create a hierarchy of responses at different temporal scales. Traits whose variation entails few transaction costs (e.g., stomatal conductance) are more likely to be shifted more frequently than those with higher costs of variation (e.g., leaf cross-sectional anatomy). The envelope of responses at the physiological and developmental time scales appears to be an important determinant of adaptive performance. However, adaptive plasticity can limit its own range of effectiveness as a consequence of energetic and competitive constraints, as seen in the allometry and zonation of emergent vs. floating aquatic plants. Plants' inherently low rate of energy capture (and, hence, developmental response and growth) and the high energetic costs of a central nervous system (CNS), may explain why they lack a brain and integrate environmental signals with a slow, hormone-based set of feedback loops rather than with a fast CNS. Finally, environmental spatial autocorrelations – especially those involving factors that determine optimal phenotype – can combine with gene flow and selection for reliance on the locally most informative signals to produce a fundamental limit on the extent of adaptive plasticity.     

Animal learning as a source of developmental bias

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path‐dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.     

Endocrine regulation of predator-induced phenotypic plasticity

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

Proteomic and gene expression differences between post-diapause and subitaneous offspring phenotypes in the cyclic parthenogen <Emphasis Type="Italic">Daphnia pulex</Emphasis>

In temperate waters, post-diapause and subitaneous offspring in Daphnia vary in life history traits and metabolic rates, and presumably are adapted to the seasonal environments in which they dwell. These offspring types result from different developmental programs of the same genetic background, representing the phenomenon of phenotypic plasticity. We aimed to explore the molecular mechanism of this phenotypic plasticity in Daphnia pulex from an intermittent population by applying a high-throughput proteomic analysis and expression analysis of several genes. The study revealed 176 proteins that were differentially expressed among offspring phenotypes. Post-diapause and subitaneous females clearly differed in their upregulated protein profiles and gene expression levels. There were more upregulated proteins with oxidoreductase and binding activity in post-diapause offspring, whereas more upregulated proteins with transporter and transferase activity were seen in subitaneous offspring. In contrast to subitaneous phenotype, over 1.5-fold more of the proteins that were upregulated in post-diapause phenotype are involved in metabolism and biosynthesis. Expression levels of several selected genes linked to cellular metabolism were also higher in post-diapause females. The greatest difference, 5-fold upregulation in post-diapause compared to subitaneous offspring, was recorded for the target of rapamycin-like (TOR) protein. Expression of ribosomal proteins in this offspring phenotype was also increased. These upregulations suggest that the TOR signaling pathway is involved and may be responsible for the regulation of the developmental program underlying post-diapause and subitaneous offspring phenotypes in Daphnia. Gene regulatory patterns observed in post-diapause and subitaneous offspring were in agreement with the expectations based on previously observed organismal traits of these Daphnia offspring types.     

Gene regulation,quantitative genetics and the evolution of reaction norms

Summary The ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.     

Developmental plasticity and evolution—quo vadis?

The role of developmental (phenotypic) plasticity in ecology and evolution is receiving a growing appreciation among the biologists, and many plasticity-specific concepts have become well established as part of the mainstream evolutionary biological thinking. In this essay, I posit that despite this progress several key perspectives in developmental plasticity remain remarkably traditional, and that it may be time to re-evaluate their continued usefulness in the face of the available evidence as the field looks to its future. Specifically, I discuss the utility of viewing plastic development as ultimately rooted in genes and genomes, and investigate the common notion that the environment—albeit a critical source of information—nevertheless remains passive, external to and separable from the organism responding to it. I end by highlighting conceptual and empirical opportunities that may permit developmental plasticity research to transcend its current boundaries and to continue its contributions toward a holistic and realistic understanding of organismal development and evolution.     

The contributions of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia

Variation among modules of a single genet could provide a means of adaptation to environmental heterogeneity. Two mechanisms that can give rise to such variation are programmed developmental change and phenotypic plasticity. I quantified the relative roles of these two mechanisms in causing within-individual variation in six leaf traits of an annual plant. Under controlled temperatures, morphological, anatomical, and physiological traits of leaves produced by the same individual differed as a function of both the node at which they were produced and the temperature they experienced during development. Temperature, node, and interactions between them all contributed significantly to the pattern of within-individual variation in leaf traits, although the relative contributions of programmed developmental change and phenotypic plasticity differed for different traits. I hypothesize that these two mechanisms for generating within-individual variation in module phenotype are favored by different patterns of environmental heterogeneity; when the sequence of environments encountered by modules of a single individual is predictable, programmed developmental change may be favored, and phenotypic plasticity may be favored when the sequence of environments is irregular with respect to individual ontogeny and therefore not predictable.