Perturbation in leaves of salt-treated Sorghum: elements for interpretation of the normal development as an adaptive response

Developmental windows are specific periods of sensitivity in which a perturbation may be adaptively integrated. In Sorghum bicolor , two developmental windows which enable adaptive adjustment to salinity (increase in tolerance) have been described during vegetative development. A third developmental window is open during the transition between vegetative and reproductive development. This third developmental window was analysed using morphological markers (specific malformations on leaves), and their relationship with vegetative and reproductive events. A positive link was observed between fertility and malformations on the last leaf. We concluded that this late window enables an adaptive adjustment of reproductive development, counteracting the negative effect of salt adaptation on fertility. Developmental windows open following rapid changes in growth of the different organs. They permit adaptive adjustments to emergence or senescence of various organs. This phenomenon is integrated within normal development, but developmental windows are enlarged for plants exposed to perturbation and for their progeny.     

Evolutionary significance of ontogenetic colour change in animals

Ontogenetic colour changes are non-reversible colour changes associated with normal progressive development of an individual of a species. This paper provides the first review of the evolutionary significance of this phenomenon in animals. Proximate mechanisms and environmental cues are briefly discussed and a conceptual framework for understanding the ultimate reasons for ontogenetic colour change is established. Changes in size, vulnerability, reproductive status, habitat and metabolism are often associated with ontogenetic colour change and can aid in understanding its adaptive significance. Neutral or non-adaptive ontogenetic colour changes due to phylogenetic inertia and developmental constraints are also considered. Existing studies of ontogenetic colour changes in marine invertebrates, terrestrial invertebrates, fish, amphibians, reptiles, birds and mammals are discussed within this framework. A need is identified for more experimental tests of hypotheses for the significance of ontogenetic colour change.     

Compensatory development and costs of plasticity: larval responses to desiccated conspecifics

Understanding constraints on phenotypic plasticity is central to explaining its evolution and the evolution of phenotypes in general, yet there is an ongoing debate on the classification and relationships among types of constraints. Since plasticity is often a developmental process, studies that consider the ontogeny of traits and their developmental mechanisms are beneficial. We manipulated the timing and reliability of cues perceived by fire salamander larvae for the future desiccation of their ephemeral pools to determine whether flexibility in developmental rates is constrained to early ontogeny. We hypothesized that higher rates of development, and particularly compensation for contradictory cues, would incur greater endogenous costs. We found that larvae respond early in ontogeny to dried conspecifics as a cue for future desiccation, but can fully compensate for this response in case more reliable but contradictory cues are later perceived. Patterns of mortality suggested that endogenous costs may depend on instantaneous rates of development, and revealed asymmetrical costs of compensatory development between false positive and false negative early information. Based on the results, we suggest a simple model of costs of development that implies a tradeoff between production costs of plasticity and phenotype-environment mismatch costs, which may potentially underlie the phenomenon of ontogenetic windows constraining plasticity.     

Examining developmental plasticity in the skeletal system through a sensitive developmental windows framework

Developmental plasticity facilitates energetically costly but potentially fitness-enhancing adjustments to phenotypic trajectories in response to environmental stressors, and thus may significantly impact patterns of growth, morbidity, and mortality over the life course. Ongoing research into epigenetics and developmental biology indicate that the timing of stress exposures is a key factor when assessing their impact on developmental processes. Specifically, stress experienced within sensitive developmental windows (SDWs), discrete developmental periods characterized by heightened energy requirements and rapid growth, may alter the pace and tempo of growth in ways that significantly influence phenotypic development over both the short and long term. In human skeletal biology, efforts to assess how developmental environments shape health outcomes over the life course could be enhanced by incorporating the SDW concept into existing methodological approaches. The goal of this article is to outline an interpretive framework for identifying and interpreting evidence of developmental stress in the skeletal system using the SDW concept. This framework provides guidance for the identification of elements most likely to capture evidence of stress most relevant to a study's core research questions, the interpretation of developmental stress exhibited by those elements, and the relationship of skeletal indicators of stress to the demographic patterning of morbidity and mortality. Use of the SDW concept in skeletal biology has the potential to enrich traditional approaches to addressing developmental origins of health and disease hypotheses, by targeting periods in which individuals are most susceptible to stress and thus most likely to exhibit plasticity in response.     

Introducing biological realism into the study of developmental plasticity in behaviour

There is increasing attention for integrating mechanistic and functional approaches to the study of (behavioural) development. As environments are mostly unstable, it is now often assumed that genetic parental information is in many cases not sufficient for offspring to become optimally adapted to the environment and that early environmental cues, either indirectly via the parents or from direct experience, are necessary to prepare them for a specific environment later in life. To study whether these early developmental processes are adaptive and through which mechanism, not only the early environmental cues but also how they impinge on the later-life environmental context has therefore to be taken into account when measuring the animal's performance. We first discuss at the conceptual level six ways in which interactions between influences of different time windows during development may act (consolidation, cumulative information gathering and priming, compensation, buffering, matching and mismatching, context dependent trait expression). In addition we discuss how different environmental factors during the same time window may interact in shaping the phenotype during development. Next we discuss the pros and cons of several experimental designs for testing these interaction effects, highlighting the necessity for full, reciprocal designs and the importance of adjusting the nature and time of manipulation to the animal's adaptive capacity. We then review support for the interaction effects from both theoretical models and animal experiments in different taxa. This demonstrates indeed the existence of interactions at multiple levels, including different environmental factors, different time windows and between generations. As a consequence, development is a life-long, environment-dependent process and therefore manipulating only the early environment without taking interaction effects with other and later environmental influences into account may lead to wrong conclusions and may also explain inconsistent results in the literature.     

Evolution and molecular mechanisms of adaptive developmental plasticity

Aside from its selective role in filtering inter-individual variation during evolution by natural selection, the environment also plays an instructive role in producing variation during development. External environmental cues can influence developmental rates and/or trajectories and lead to the production of distinct phenotypes from the same genotype. This can result in a better match between adult phenotype and selective environment and thus represents a potential solution to problems posed by environmental fluctuation. The phenomenon is called adaptive developmental plasticity. The study of developmental plasticity integrates different disciplines (notably ecology and developmental biology) and analyses at all levels of biological organization, from the molecular regulation of changes in organismal development to variation in phenotypes and fitness in natural populations. Here, we focus on recent advances and examples from morphological traits in animals to provide a broad overview covering (i) the evolution of developmental plasticity, as well as its relevance to adaptive evolution, (ii) the ecological significance of alternative environmentally induced phenotypes, and the way the external environment can affect development to produce them, (iii) the molecular mechanisms underlying developmental plasticity, with emphasis on the contribution of genetic, physiological and epigenetic factors, and (iv) current challenges and trends, including the relevance of the environmental sensitivity of development to studies in ecological developmental biology, biomedicine and conservation biology.     

The thrifty phenotype as an adaptive maternal effect

Human diseases in adulthood are increasingly associated with growth patterns in early life, implicating early-life nutrition as the underlying mechanism. The thrifty phenotype hypothesis proposed that early-life metabolic adaptations promote survival, with the developing organism responding to cues of environmental quality by selecting an appropriate trajectory of growth. Recently, some authors have proposed that the thrifty phenotype is also adaptive in the longer-term, by preparing the organism for its likely adult environment. However, windows of plasticity close early during human development, and subsequent environmental changes may result in the selected trajectory becoming inappropriate, leading to adverse effects on health. This paradox generates uncertainty as to whether the thrifty phenotype is indeed adaptive for the offspring in humans. The thrifty phenotype should not be considered a dichotomous concept, rather it refers to the capacity of all offspring to respond to environmental information during early ontogenetic development. This article argues that the thrifty phenotype is the consequence of three different adaptive processes - niche construction, maternal effects, and developmental plasticity - all of which in humans are influenced by our large brains. While developmental plasticity represents an adaptation by the offspring, both niche construction and parental effects are subject to selection on parental rather than offspring fitness. The three processes also operate at different paces. Human offspring do not become net calories-producers until around 18 years of age, such that the high energy costs of the human brain are paid primarily by the mother, even after weaning. The evolutionary expansion of human brain volume occurred in environments characterised by high volatility, inducing strong selective pressure on maternal capacity to provision multiple offspring simultaneously. The thrifty phenotype is therefore best considered as a manipulation of offspring phenotype for the benefit of maternal fitness. The information that enters offspring phenotype during early development does not predict the likely future environment of the offspring, but rather reflects the mother's own developmental experience and the quality of the environment during her own maturation. Offspring growth trajectory thus becomes aligned with long-term maternal capacity to provision. In contemporary populations, the sensitivity of offspring development to maternal phenotype exposes the offspring to adverse effects, through four distinct pathways. The offspring may be exposed to (1) poor maternal metabolic control (e.g. gestational diabetes), (2) maternally derived toxins (e.g. maternal smoking), or (3) low maternal social status (e.g. small size). Adverse consequences of these effects may then be exacerbated by (4) exposure either to the "toxic" western environment in postnatal life, in which diet and physical activity levels are mismatched with metabolic experience in utero, or at the other extreme to famine. The rapid emergence of the epidemic of the metabolic syndrome in the 20th Century reflects the rapid acceleration in the pace of niche construction relative to the slower physiological combination of developmental plasticity and parental effects.     

Can environmental conditions experienced in early life influence future generations?

The consequences of early developmental conditions for performance in later life are now subjected to convergent interest from many different biological sub-disciplines. However, striking data, largely from the biomedical literature, show that environmental effects experienced even before conception can be transmissible to subsequent generations. Here, we review the growing evidence from natural systems for these cross-generational effects of early life conditions, showing that they can be generated by diverse environmental stressors, affect offspring in many ways and can be transmitted directly or indirectly by both parental lines for several generations. In doing so, we emphasize why early life might be so sensitive to the transmission of environmentally induced effects across generations. We also summarize recent theoretical advancements within the field of developmental plasticity, and discuss how parents might assemble different ‘internal’ and ‘external’ cues, even from the earliest stages of life, to instruct their investment decisions in offspring. In doing so, we provide a preliminary framework within the context of adaptive plasticity for understanding inter-generational phenomena that arise from early life conditions.     

Neuronal cytoskeleton in synaptic plasticity and regeneration

During development, dynamic changes in the axonal growth cone and dendrite are necessary for exploratory movements underlying initial axo‐dendritic contact and ultimately the formation of a functional synapse. In the adult central nervous system, an impressive degree of plasticity is retained through morphological and molecular rearrangements in the pre‐ and post‐synaptic compartments that underlie the strengthening or weakening of synaptic pathways. Plasticity is regulated by the interplay of permissive and inhibitory extracellular cues, which signal through receptors at the synapse to regulate the closure of critical periods of developmental plasticity as well as by acute changes in plasticity in response to experience and activity in the adult. The molecular underpinnings of synaptic plasticity are actively studied and it is clear that the cytoskeleton is a key substrate for many cues that affect plasticity. Many of the cues that restrict synaptic plasticity exhibit residual activity in the injured adult CNS and restrict regenerative growth by targeting the cytoskeleton. Here, we review some of the latest insights into how cytoskeletal remodeling affects neuronal plasticity and discuss how the cytoskeleton is being targeted in an effort to promote plasticity and repair following traumatic injury in the central nervous system.     

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.     

Intrinsic and environmental response pathways that regulate root system architecture

Root system development is an important agronomic trait. The right architecture in a given environment allows plants to survive periods of water of nutrient deficit, and compete effectively for resources. Root systems also provide an optimal system for studying developmental plasticity, a characteristic feature of plant growth. This review proposes a framework for describing the pathways regulating the development of complex structures such as root systems: intrinsic pathways determine the characteristic architecture of the root system in a given plant species, and define the limits for plasticity in that species. Response pathways co-ordinate environmental cues with development by modulating intrinsic pathways. The current literature describing the regulation of root system development is summarized here within this framework. Regulatory pathways are also organized based on their specific developmental effect in the root system. All the pathways affect lateral root formation, but some specifically target initiation of the lateral root, while others target the development and activation of the lateral root primordium, or the elongation of the lateral root. Finally, we discuss emerging approaches for understanding the regulation of root system architecture.     

Neuroplasticity in respiratory motor control.

Although recent evidence demonstrates considerable neuroplasticity in the respiratory control system, a comprehensive conceptual framework is lacking. Our goals in this review are to define plasticity (and related neural properties) as it pertains to respiratory control and to discuss potential sites, mechanisms, and known categories of respiratory plasticity. Respiratory plasticity is defined as a persistent change in the neural control system based on prior experience. Plasticity may involve structural and/or functional alterations (most commonly both) and can arise from multiple cellular/synaptic mechanisms at different sites in the respiratory control system. Respiratory neuroplasticity is critically dependent on the establishment of necessary preconditions, the stimulus paradigm, the balance between opposing modulatory systems, age, gender, and genetics. Respiratory plasticity can be induced by hypoxia, hypercapnia, exercise, injury, stress, and pharmacological interventions or conditioning and occurs during development as well as in adults. Developmental plasticity is induced by experiences (e.g., altered respiratory gases) during sensitive developmental periods, thereby altering mature respiratory control. The same experience later in life has little or no effect. In adults, neuromodulation plays a prominent role in several forms of respiratory plasticity. For example, serotonergic modulation is thought to initiate and/or maintain respiratory plasticity following intermittent hypoxia, repeated hypercapnic exercise, spinal sensory denervation, spinal cord injury, and at least some conditioned reflexes. Considerable work is necessary before we fully appreciate the biological significance of respiratory plasticity, its underlying cellular/molecular and network mechanisms, and the potential to harness respiratory plasticity as a therapeutic tool.     

A new perspective on developmental plasticity and the principles of adaptive morph determination

Organisms can have divergent paths of development leading to alternative phenotypes, or morphs. The choice of developmental path may be set by environmental cues, the individual's genotype, or a combination of the two. Using individual-based simulation and analytical investigation, we explore the idea that from the viewpoint of a developmental switch, genetic morph determination can sometimes be regarded as adaptive developmental plasticity. We compare the possibilities for the evolution of environmental and genetic morph determination and combinations of the two in situations with spatial variation in conditions. We find that the accuracy of environmental cues in predicting coming selective conditions is important for environmental morph determination, in accordance with previous results, and that genetic morph determination is favored in a similar way by the accuracy of genetic cues, in the form of selectively maintained gene frequency differences between local populations. Restricted gene flow and strong selection acting on the phenotypic alternatives produce clearer gene frequency differences and lead to greater accuracy of genetic cues. For combined environmental and genetic morph determination, we show that the developmental machinery can evolve toward efficiently combining information in environmental and genetic cues for the purpose of predicting coming selective conditions.     

Selective processes in development: implications for the costs and benefits of phenotypic plasticity

Adaptive phenotypic plasticity, the ability of a genotype to develop a phenotype appropriate to the local environment, allows organisms to cope with environmental variation and has implications for predicting how organisms will respond to rapid, human-induced environmental change. This review focuses on the importance of developmental selection, broadly defined as a developmental process that involves the sampling of a range of phenotypes and feedback from the environment reinforcing high-performing phenotypes. I hypothesize that understanding the degree to which developmental selection underlies plasticity is key to predicting the costs, benefits, and consequences of plasticity. First, I review examples that illustrate that elements of developmental selection are common across the development of many different traits, from physiology and immunity to circulation and behavior. Second, I argue that developmental selection, relative to a fixed strategy or determinate (switch) mechanisms of plasticity, increases the probability that an individual will develop a phenotype best matched to the local environment. However, the exploration and environmental feedback associated with developmental selection is costly in terms of time, energy, and predation risk, resulting in major changes in life history such as increased duration of development and greater investment in individual offspring. Third, I discuss implications of developmental selection as a mechanism of plasticity, from predicting adaptive responses to novel environments to understanding conditions under which genetic assimilation may fuel diversification. Finally, I outline exciting areas of future research, in particular exploring costs of selective processes in the development of traits outside of behavior and modeling developmental selection and evolution in novel environments.     

Mechanisms of experience-dependent plasticity in the auditory localization pathway of the barn owl

Sound localization is a computational process that requires the central nervous system to measure various auditory cues and then associate particular cue values with appropriate locations in space. Behavioral experiments show that barn owls learn to associate values of cues with locations in space based on experience. The capacity for experience-driven changes in sound localization behavior is particularly great during a sensitive period that lasts until the approach of adulthood. Neurophysiological techniques have been used to determine underlying sites of plasticity in the auditory space-processing pathway. The external nucleus of the inferior colliculus (ICX), where a map of auditory space is synthesized, is a major site of plasticity. Experience during the sensitive period can cause large-scale, adaptive changes in the tuning of ICX neurons for sound localization cues. Large-scale physiological changes are accompanied by anatomical remodeling of afferent axons to the ICX. Changes in the tuning of ICX neurons for cue values involve two stages: (1) the instructed acquisition of neuronal responses to novel cue values and (2) the elimination of responses to inappropriate cue values. Newly acquired neuronal responses depend differentially on NMDA receptor currents for their expression. A model is presented that can account for this adaptive plasticity in terms of plausible cellular mechanisms. Accepted: 17 April 1999     

Clutch identity and predator-induced hatching affect behavior and development in a leaf-breeding treefrog

For species with complex life cycles, transitions between life stages result in niche shifts that are often associated with evolutionary trade-offs. When conditions across life stages are unpredictable, plasticity in niche shift timing may be adaptive; however, factors associated with clutch identity (e.g., genetic or maternal) may influence the effects of such plasticity. The red-eyed treefrog (Agalychnis callidryas) is an ideal organism for investigating the effects of genetics and life stage switch point timing because embryos exhibit adaptive phenotypic plasticity in hatching time. In this study, we evaluated the effects of experimentally manipulated hatching time and clutch identity on antipredator behavior of tadpoles and on developmental traits of metamorphs, including larval period, mass, SVL, and jumping ability. We found that in the presence of dragonfly nymph predator cues at 21 days post-oviposition, tadpoles reduced both their activity level and height in the water column. Furthermore, early-hatched tadpoles were less active than late-hatched tadpoles of the same age. This difference in behavior patterns of early- and late-hatched tadpoles may represent an adaptive response due to a longer period of susceptibility to odonate predators for early-hatched tadpoles, or it may be a carry-over effect mediated by early exposure to an environmental stressor (i.e., induction of early hatching). We also found that hatching time affected both behavioral traits and developmental traits, but its effect on developmental traits varied significantly among clutches. This study shows that a single early-life event may influence a suite of factors during subsequent life stages and that some of these effects appear to be dependent on clutch identity. This interaction may represent an evolutionary response to a complex life cycle and unpredictable environments, regardless of whether the clutch differences are due to additive genetic variance or maternal effects.     

The lost generation hypothesis: could climate change drive ectotherms into a developmental trap?

Climate warming affects the rate and timing of the development in ectothermic organisms. Short‐living, ectothermic organisms (including many insects) showing thermal plasticity in life‐cycle regulation could, for example, increase the number of generations per year under warmer conditions. However, changed phenology may challenge the way organisms in temperate climates deal with the available thermal time window at the end of summer. Although adaptive plasticity is widely assumed in multivoltine organisms, rapid environmental change could distort the quality of information given by environmental cues that organisms use to make developmental decisions. Developmental traps are scenarios in which rapid environmental change triggers organisms to pursue maladaptive developmental pathways. This occurs because organisms must rely upon current environmental cues to predict future environmental conditions and corresponds to a novel case of ecological or evolutionary traps. Examples of introduced, invasive species are congruent with this hypothesis. Based on preliminary experiments, we argue that the dramatic declines of the wall brown Lasiommata megera in northwestern Europe may be an example of a developmental trap. This formerly widespread, bivoltine (or even multivoltine) butterfly has become a conundrum to conservationist biologists. A split‐brood field experiment with L. megera indeed suggests issues with life‐cycle regulation decisions at the end of summer. In areas where the species went extinct recently, 100% of the individuals developed directly into a third generation without larval diapause, whereas only 42.5% did so in the areas where the species still occurs. Under unfavourable autumn conditions, the attempted third generation will result in high mortality and eventually a lost or ‘suicidal’ third generation in this insect with non‐overlapping, discrete generations. We discuss the idea of a developmental trap within an integrated framework for assessing the vulnerability of species to climate change.     

Environmental and genetic cues in the evolution of phenotypic polymorphism

Phenotypic polymorphism is a consequence of developmental plasticity, in which the trajectories of developing organisms diverge under the influence of cues. Environmental and genetic phenotype determination are the two main categories of polymorphic development. Even though both may evolve as a response to varied environments, they are traditionally regarded as fundamentally distinct phenomena. They can however be joined into a single framework that emphasizes the parallel roles of environmental and genetic cues in phenotype determination. First, from the point of view of immediate causation, it is common that phenotypic variants can be induced either by environmental or by allelic variation, and this is referred to as gene-environment interchangeability. Second, from the point of view of adaptation, genetic cues in the form of allelic variation at polymorphic loci can play similar roles as environmental cues in providing information to the developmental system about coming selective conditions. Both types of cues can help a developing organism to fit its phenotype to selective circumstances. This perspective of information in environmental and genetic cues can produce testable hypotheses about phenotype determination, and can thus increase our understanding of the evolution of phenotypic polymorphism.     

Influence of the environment on adult CNS plasticity and repair

During developmental critical periods, external stimuli are crucial for information processing, acquisition of new functions or functional recovery after CNS damage. These phenomena depend on the capability of neurons to modify their functional properties and/or their connections, generally defined as "plasticity". Although plasticity decreases after the closure of critical periods, the adult CNS retains significant capabilities for structural remodelling and functional adaptation. At the molecular level, structural modifications of neural circuits depend on the balance between intrinsic growth properties of the involved neurons and growth-regulatory cues of the extracellular milieu. Interestingly, experience acts on this balance, so as to create permissive conditions for neuritic remodelling. Here, we present an overview of recent findings concerning the effects of experience on cellular and molecular processes responsible for producing structural plasticity of neural networks or functional recovery after an insult to the adult CNS (e.g. traumatic injury, ischemia or neurodegenerative disease). Understanding experience-dependent mechanisms is crucial for the development of tailored rehabilitative strategies, which can be exploited alone or in combination with specific therapeutic interventions to improve neural repair after damage.