Form Of Developmental Plasticity Research Articles

How important is hidden phenotypic plasticity arising from alternative but converging developmental trajectories, and what limits it?

Developmental plasticity -- the capacity for a genotype to develop into different phenotypes, depending on the environment - is typically viewed from the perspective of the resulting phenotype. Thus, if development is viewed as a trajectory towards a target, then developmental plasticity allows environmentally induced alterations to the target. However, there can also be variations in the trajectory. This is seen with compensatory responses, for instance where growth accelerates after an earlier period of food shortage, or where investment in sexual ornaments is maintained even when resources are limiting. If the compensation is complete, the adult phenotype can appear 'normal' (i.e. the different developmental trajectories converge on the same target). However, alternative trajectories to a common target can have multiple long-term consequences, including altered physiological programming and rates of senescence, possibly owing to trade-offs between allocating resources to the prioritized trait versus to body maintenance. This suggests that plasticity in developmental trajectories towards a common target leads to variation in the resilience and robustness of the adult body. This form of developmental plasticity is far more hidden than plasticity in final adult target, but it may be more common. Here, I discuss the causes, consequences and limitations of these different kinds of plasticity, with a special focus on whether they are likely to be adaptive. I emphasize the need to study plasticity in developmental trajectories, and conclude with suggestions for future research to tease apart the different forms of developmental plasticity and the factors that influence their evolution and expression.

About the Cover

Next article FreeAbout the CoverPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinked InRedditEmailQR Code SectionsMoreThe cover image features a hatchling American alligator (Alligator mississippiensis) emerging from its nest. Like many non-mammalian vertebrates, the temperature that alligators experience during development determines their sex. Temperature-dependent sex determination (TSD) is a form of developmental plasticity that may provide insight into how taxa respond to fluctuating environments and extreme conditions that are predicted to intensify with ongoing climate change. However, the evolutionary drivers of TSD are unresolved for many species, including crocodilians. In this issue, S. L. Bock, M. D. Hale, T. R. Rainwater, P. M. Wilkinson, and B. B. Parrott (pp. 43–54) demonstrate that fluctuating versus constant temperature conditions have different effects on the juvenile phenotype of alligators, and that warmer temperatures produce males with greater residual yolk reserves and larger hatchling sizes. Variation in developmental costs at different incubation temperatures may therefore contribute to the evolution of TSD.Coastal ecosystems are naturally variable in important physical stressors like temperature, salinity, pH, and hypoxia. Understanding how species adapt to such fluctuating conditions should enable better predictions of the evolutionary responses of coastal communities to climate change. In their Introduction (pp. 1–3), the editors of the series—Patrick J. Krug, John P. Wares, and Jonathan D. Allen—argue for a broader study of plasticity and local adaptation in aquatic organisms in the context of a fast-changing climate. This symposium issue brings together contributions examining all life stages of freshwater, estuarine, and marine organisms and uses approaches ranging from genomic to experimental techniques to understand survival strategies in unpredictable versus stable environments.Credits: Photo of juvenile alligator, Benjamin B. Parrott, Odum School of Ecology, University of Georgia. Cover design, Matt Lang, University of Chicago Press. Next article DetailsFiguresReferencesCited by The Biological Bulletin Volume 241, Number 1August 2021Adaptive and Plastic Responses to Environmental Variation Published in association with the Marine Biological Laboratory Article DOIhttps://doi.org/10.1086/717022 Views: 304 © 2021 by The University of Chicago. All rights reserved.PDF download Crossref reports no articles citing this article.

A model of optimal timing for a predictive adaptive response.

Predictive adaptive responses (PARs) are a form of developmental plasticity in which the developmental response to an environmental cue experienced early in life is delayed and yet, at the same time, the induced phenotype anticipates (i.e., is completely developed before) exposure to the eventual environmental state predicted by the cue, in which the phenotype is adaptive. We model this sequence of events to discover, under various assumptions concerning the cost of development, what lengths of delay, developmental time, and anticipation are optimal. We find that in many scenarios modeled, development of the induced phenotype should be completed at the exact same time that the environmental exposure relevant to the induced phenotype begins: that is, in contrast to our observed cases of PARs, there should be no anticipation. Moreover, unless slow development is costly, development should commence immediately after the cue: there should be no delay. Thus, PARs, which normally have non-zero delays and/or anticipation, are highly unusual. Importantly, the exceptions to these predictions of zero delays and anticipation occurred when developmental time was fixed and delaying development was increasingly costly. We suggest, therefore, that PARs will only evolve under three kinds of circumstances: (i) there are strong timing constraints on the cue and the environmental status, (ii) delaying development is costly, and development time is either fixed or slow development is costly, or (iii) when the period between the cue and the eventual environmental change is variable and the cost of not completing development before the change is high. These predictions are empirically testable.

Influence of chronic hyperoxia on the developmental time course of the hypoxic ventilatory response relative to other traits in rats

Newborn mammals exhibit a biphasic hypoxic ventilatory response (HVR) in which an initial increase in ventilation is followed by a decline back toward baseline levels. The magnitude of the secondary decline diminishes with postnatal age, but this transition occurs earlier in rat pups reared in moderate hyperoxia. This pattern is consistent with heterokairy, a form of developmental plasticity in which environmental factors alter the timing of developmental events. The present study investigated whether this plasticity is specific to the HVR or if hyperoxia instead accelerates overall development. Rat pups reared in 60 % O2 (Hyperoxia) exhibited a less biphasic ventilatory response to 12 % O2 than pups reared in 21 % O2 (Control) at 4 days of age (P4) and transitioned to a sustained HVR by P10-11; Control rats exhibited a biphasic HVR at both ages. However, the average ages at which pups attained other key developmental milestones (i.e., fur development at P5, incisor eruption at P9, and eye opening at P15) were similar between treatment groups. Moreover, growth rates and maturation of the metabolic response to cooling were not accelerated, and may have been delayed slightly, relative to Control rats. For example, the capacity for pups to increase their metabolic rate at low ambient temperatures increased with age, but this thermogenic capacity tended to be reduced in Hyperoxia pups at both P4 and P10-11 (i.e., lower CO2 production rates below the lower critical temperature). Collectively, these data support the conclusion that hyperoxia specifically advances the age at which rat pups exhibit a sustained HVR, altering the relative timing of developmental events rather than compressing the entire period of development.

Early Maturation of the Hypoxic Ventilatory Response in Hyperoxic Rat Pups: Evidence for Trait‐Specific Heterokairy

Newborn mammals exhibit a biphasic hypoxic ventilatory response (HVR) in which an initial increase in ventilation is followed by a decline back toward baseline levels. The magnitude of the secondary decline diminishes with age, but rat pups reared in moderate hyperoxia make this transition earlier (Bavis et al., J. Appl. Physiol. 109(3): 796–803, 2010). This is consistent with heterokairy, a form of developmental plasticity in which environmental factors alter the rate and/or timing of developmental events. The present study investigated whether this effect is specific to the HVR or if hyperoxia instead accelerates overall development. Rat pups reared in 60% O2 (Hyperoxia) exhibited a less biphasic HVR at both P4 and P10‐11 compared to pups reared in 21% O2 (Control). However, growth curves and the average ages at which pups attained key developmental milestones (i.e., fur development at P5, incisor eruption at P9, and eye opening at P15) were similar between treatment groups. We also studied the relationship between metabolic rate and ambient temperature as another indicator of physiological maturity. The lower critical temperature (LCT) decreased with age, but the LCT was the same for Control and Hyperoxia rats at both P4 (~32°C) and P10‐11 (~30°C). The ability to increase metabolic rate at low ambient temperatures also increased with age, but this thermogenic capacity tended to be reduced in Hyperoxia rats at both P4 and P10‐11 (i.e., lower rates of metabolic CO2 production at temperatures below the LCT). We conclude that hyperoxia accelerates the rate at which the HVR matures without affecting the maturation of other morphological and physiological traits.

Regulators of an ancient polyphenism evolved through episodic protein divergence and parallel gene radiations.

Polyphenism is a form of developmental plasticity that transduces environmental cues into discontinuous, often disparate phenotypes. In some cases, polyphenism has been attributed to facilitating morphological diversification and even the evolution of novel traits. However, this process is predicated on the origins and evolutionary maintenance of genetic mechanisms that specify alternate developmental networks. When and how regulatory loci arise and change, specifically before and throughout the history of a polyphenism, is little understood. Here, we establish a phylogenetic and comparative molecular context for two dynamically evolving genes, eud-1 and seud-1, which regulate polyphenism in the nematode Pristionchus pacificus. This species is dimorphic in its adult feeding-structures, allowing individuals to become microbivores or facultative predators depending on the environment. Although polyphenism regulation is increasingly well understood in P. pacificus, the polyphenism is far older than this species and has diversified morphologically to enable an array of ecological functions across polyphenic lineages. To bring this taxonomic diversity into a comparative context, we reconstructed the histories of eud-1 and seud-1 relative to the origin and diversification of polyphenism, finding that homologues of both genes have undergone lineage-specific radiations across polyphenic taxa. Further, we detected signatures of episodic diversifying selection on eud-1, particularly in early diplogastrid lineages. Lastly, transgenic rescue experiments suggest that the gene's product has functionally diverged from its orthologue's in a non-polyphenic outgroup. In summary, we provide a comparative framework for the molecular components of a plasticity switch, enabling studies of how polyphenism, its regulation, and ultimately its targets evolve.

Developmental Stage Affects the Consequences of Transient Salinity Exposure in Toad Tadpoles.

Development can play a critical role in how organisms respond to changes in the environment. Tolerance to environmental challenges can vary during ontogeny, with individual- and population-level impacts that are associated with the timing of exposure relative to the timing of vulnerability. In addition, the life history consequences of different stressors can vary with the timing of exposure to stress. Salinization of freshwater ecosystems is an emerging environmental concern, and habitat salinity can change rapidly due, for example, to storm surge, runoff of road deicing salts, and rainfall. Elevated salinity can increase the demands of osmoregulation in freshwater organisms, and amphibians are particularly at risk due to their permeable skin and, in many species, semi-aquatic life cycle. In three experiments, we manipulated timing and duration of exposure to elevated salinity during larval development of southern toad (Anaxyrus terrestris) tadpoles and examined effects on survival, larval growth, and timing of and size at metamorphosis. Survival was reduced only for tadpoles exposed to elevated salinity early in development, suggesting an increase in tolerance as development proceeds; however, we found no evidence of acclimation to elevated salinity. Two forms of developmental plasticity may help to ameliorate costs of transient salinity exposure. With early salinity exposure, the return to freshwater was accompanied by a period of rapid compensatory growth, and metamorphosis ultimately occurred at a similar age and size as freshwater controls. By contrast, salinity exposure later in development led to earlier metamorphosis at reduced size, indicating an acceleration of metamorphosis as a mechanism to escape salinity stress. Thus, the consequences of transient salinity exposure were complex and were mediated by developmental state. Salinity stress experienced early in development resulted in acute costs but little long-lasting effect on survivors, while exposures later in development resulted in sublethal effects that could influence success in subsequent life stages. Overall, our results suggest that elevated salinity is more likely to affect southern toad larvae when experienced early during larval development, but even brief sublethal exposure later in development can alter life history in ways that may impact fitness.

Novel host plant leads to the loss of sexual dimorphism in a sexually selected male weapon.

In this time of massive global change, species are now frequently interacting with novel players. Greater insight into the impact of these novel interactions on traits linked to fitness is essential, because effects on these traits can hinder population existence or promote rapid adaptation. Sexually selected weapons and ornaments frequently influence fitness and often have heightened condition-dependence in response to nutrition. Condition-dependence in response to different ecological conditions, a form of developmental plasticity, may be responsible for much of the intraspecific variation in sexually selected ornaments and weapons in wild populations. Here we examined the consequences of developing on a novel plant for the expression of size and shape in the leaf-footed cactus bug Narnia femorata (Hemiptera: Coreidae). The males of this species possess enlarged, sexually dimorphic femurs on their hind legs. These legs are used as weapons in male-male contests. Females are typically larger in overall body size. Our study revealed that developing upon a novel host can lead to pronounced phenotypically plastic change in sexually dimorphic traits. Male hind femurs were greatly impacted by the novel diet to the extent that the sexual dimorphism in hind femurs was lost. Further, dimorphism in body size increased, as males became tiny adults while females better maintained their body size. These patterns underscore the complex effects that novel species interactions may have on sexual phenotypes.

Somato-dendritic decoupling as a novel mechanism for protracted cortical maturation.

BackgroundBoth human and animal data indicate that disruption of the endogenously slow maturation of temporal association cortical (TeA) networks is associated with abnormal higher order cognitive development. However, the neuronal mechanisms underlying the endogenous maturation delay of the TeA are poorly understood.ResultsHere we report a novel form of developmental plasticity that is present in the TeA. It was found that deep layer TeA neurons, but not hippocampal or primary visual neurons, exist in a protracted ’embryonic-like’ state through a mechanism involving reduced somato-dendritic communication and a non-excitable somatic membrane. This mechanism of neural inactivity is present in intact tissue and shows a remarkable transition into an active somato-dendritically coupled state. The quantity of decoupled cells diminishes in a protracted and age-dependent manner, continuing into adolescence.ConclusionsBased on our data, we propose a model of neural plasticity through which protracted compartmentalization and decoupling in somato-dendritic signalling plays a key role in controlling how excitable neurons are incorporated into recurrent cortical networks independent of neurogenesis.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0270-5) contains supplementary material, which is available to authorized users.

Development of Dive Capacity in Northern Elephant Seals (Mirounga angustirostris): Reduced Body Reserves at Weaning Are Associated with Elevated Body Oxygen Stores during the Postweaning Fast.

Developmental increases in dive capacity have been reported in numerous species of air-breathing marine vertebrates. Previous studies in juvenile phocid seals suggest that increases in physiological dive capacity during the postweaning fast (PWF) are critical to support independent aquatic foraging. Although there is a strong relationship between size at weaning and PWF duration and body reserves at weaning vary considerably, few studies have considered whether such variation in body reserve magnitude promotes phenotypic modulation of dive capacity development during the PWF. Phenotypic modulation, a form of developmental plasticity in which rates and degrees of expression of the developmental program are modulated by environmental factors, may enhance diving capacity in weanlings with reduced PWF durations due to smaller body reserves at weaning if reduced body reserves promote accelerated development of dive capacity. We longitudinally measured changes in blood and muscle oxygen stores and muscle metabolic enzymes over the first 8 wk of the PWF in northern elephant seals and determined whether rates of change in these parameters varied with body reserves at weaning. We assessed whether erythropoietin (EPO), thyroid hormones, serum nonesterified fatty acid levels, and iron status influenced blood and muscle oxygen store development or were influenced by body reserves at weaning. Although mass-specific plasma volume and blood volume were relatively stable across the fast, both were elevated in animals with reduced body reserves. Surprisingly, hemoglobin and mean corpuscular hemoglobin concentrations declined over the PWF while hematocrit remained stable, and these variables were not associated with body reserves or EPO. Swimming muscle myoglobin and serum iron levels increased rapidly early in the PWF and were not related to body reserves. Patterns in maximal activities of muscle enzymes suggested a decline in total aerobic and anaerobic metabolic capacity over the PWF, despite maintenance of fat oxidation capacity. These results suggest that only development of blood volume is increased in smaller weanlings and that extended fasting durations in larger weanlings do not improve physiological dive capacity.

Skeletal remodelling suggests the turtle's shell is not an evolutionary straitjacket.

Recent efforts to decipher the enigma of the turtle's shell revealed that distantly related turtle species deploy diverse processes during shell development. Even so, extant species share in common a shoulder blade (scapula) that is encapsulated within the shell. Thus, evolutionary change in the correlated development of the shell and scapula probably underpins the evolution of highly derived shell morphologies. To address this expectation, we conducted one of the most phylogenetically comprehensive surveys of turtle development, focusing on scapula growth and differentiation in embryos, hatchlings and adults of 13 species. We report, to our knowledge, the first description of secondary differentiation owing to skeletal remodelling of the tetrapod scapula in turtles with the most structurally derived shell phenotypes. Remodelling and secondary differentiation late in embryogenesis of box turtles (Emys and Terrapene) yielded a novel skeletal segment (i.e. the suprascapula) of high functional value to their complex shell-closing system. Remarkably, our analyses suggest that, in soft-shelled turtles (Trionychidae) with extremely flattened shells, a similar transformation is linked to truncated scapula growth. Skeletal remodelling, as a form of developmental plasticity, might enable the seemingly constrained turtle body plan to diversify, suggesting the shell is not an evolutionary straitjacket.

Conrad Waddington and the origin of epigenetics.

Denis Noble discusses Conrad Waddington's classic paper, "The genetic assimilation of the bithorax phenotype", published in Evolution in 1956.

Extracellular matrix molecules, their receptors, and secreted proteases in synaptic plasticity

Neural cells secrete diverse molecules, which accumulate in the extracellular space and form the extracellular matrix (ECM). Interactions between cells and the ECM are well recognized to play the crucial role in cell migration and guidance of growing axons, whereas formation of mature neural ECM in the form of perineuronal nets is believed to restrict certain forms of developmental plasticity. On the other hand, major components of perineuronal nets and other ECM molecules support induction of functional plasticity, the most studied form of which is long-term potentiation. Here, we review the underlying mechanisms by which ECM molecules, their receptors and remodeling proteases regulate the induction and maintenance of synaptic modifications. In particular, we highlight that activity-dependent secretion and activation of proteases leads to a local cleavage of the ECM and release of signaling proteolytic fragments. These molecules regulate transmitter receptor trafficking, actin cytoskeleton, growth of dendritic spines, and formation of dendritic filopodia.

Critical Period Plasticity Is Disrupted in the Barrel Cortex of Fmr1 Knockout Mice

Alterations in sensory processing constitute prominent symptoms of fragile X syndrome; however, little is known about how disrupted synaptic and circuit development in sensory cortex contributes to these deficits. To investigate how the loss of fragile X mental retardation protein (FMRP) impacts the development of cortical synapses, we examined excitatory thalamocortical synapses in somatosensory cortex during the perinatal critical period in Fmr1 knockout mice. FMRP ablation resulted in dysregulation of glutamatergic signaling maturation. The fraction of silent synapses persisting to later developmental times was increased; there was a temporal delay in the window for synaptic plasticity, while other forms of developmental plasticity were not altered in Fmr1 knockout mice. Our results indicate that FMRP is required for the normal developmental progression of synaptic maturation, and loss of this important RNA binding protein impacts the timing of the critical period for layer IV synaptic plasticity.

Developmental switch from GABA to glycine release in single central synaptic terminals

Early in postnatal development, inhibitory inputs to rat lateral superior olive (LSO) neurons change from releasing predominantly GABA to releasing predominantly glycine into the synapse. Here we show that spontaneous miniature inhibitory postsynaptic currents (mIPSCs) also change from GABAergic to glycinergic over the first two postnatal weeks. Many 'mixed' mIPSCs, resulting from co-release of glycine and GABA from the same vesicles, are seen during this transition. Immunohistochemistry showed that a large number of terminals contained both GABA and glycine at postnatal day 8 (P8). By P14, both the content of GABA in these mixed terminals and the contribution of GABA to the mixed mIPSCs had decreased. The content of glycine in terminals increased over the same period. Our results indicate that switching from GABAergic to glycinergic inputs to the LSO may occur at the level of a single presynaptic terminal. This demonstrates a new form of developmental plasticity at the level of a single central synapse.

Developing mechanisms of self-regulation.

Child development involves both reactive and self-regulatory mechanisms that children develop in conjunction with social norms. A half-century of research has uncovered aspects of the physical basis of attentional networks that produce regulation, and has given us some knowledge of how the social environment may alter them. In this paper, we discuss six forms of developmental plasticity related to aspects of attention. We then focus on effortful or executive aspects of attention, reviewing research on temperamental individual differences and important pathways to normal and pathological development. Pathologies of development may arise when regulatory and reactive systems fail to reach the balance that allows for both self-expression and socially acceptable behavior. It remains a challenge for our society during the next millennium to obtain the information necessary to design systems that allow a successful balance to be realized by the largest possible number of children.

Ready and Waiting: Delayed Hatching and Extended Incubation of Anamniotic Vertebrate Terrestrial Eggs

Some anamniotic aquatic vertebrates lay eggs in a terrestrial habitat that is hostile to the survival of hatchings or larvae. These terrestrial eggs are ready and able to hatch at a particular developmental time, but do not hatch until presented with suitable conditions for aquatic larval survival. Beyond this time, hatching is possible whenever aquatic conditions occur. The duration of extended terrestrial incubation is dependent on the availability of energy for metabolism from the yolk. Extended incubation is useful for anamniotic eggs laid in terrestrial habitats where conditions suitable for larval survival arrive with unpredictable or variable timing. Examples of anamniotes with delayed hatching and extended terrestrial incubation can be found among teleost fishes, anurans, and caudate amphibians. This paper characterizes the embryonic period, compares this mode with other forms of developmental plasticity in anamniotes, evaluates the constraints and advantages of this life history mode, and examines how some fishes and amphibians are able to obtain the benefits of terrestriality for their eggs when the timing of the return to aquatic conditions is not entirely predictable.

Anatomical and synaptic substrates for avian song learning.

In songbirds, vocal learning occurs during periods of major cellular and synaptic change. This neural reorganization includes massive synaptogenesis associated with the addition of new neurons into the vocal motor pathway, as well as pruning of connections between song regions. These observations, coupled with behavioral evidence that song development requires NMDA receptor activation in specific song nuclei, suggest that experiences associated with vocal learning are encoded by activity driven, Hebbianlike processes of synaptic change akin to those implicated in many other forms of developmental plasticity and learning. In this review we discuss the hypothesis that develpmental and/or seasonal changes in NMDA receptor function and the availability of new synapses may modulate thresholds for plasticity and thereby define sensitive periods for vocal learning.

Action-Based Learning: a New Form of Developmental Plasticity in Bird Song

Two forms of developmental plasticity in bird song are contrasted. The classical 'memory-based' or sensorimotor process includes a sensory phase during which a song model is memorized followed by a motor phase during which the bird matches his own song to the model via auditory feedback. In contrast, 'action-based learning' refers to the selection of songs that are already produced for retention in the mature repertoire. Evidence for action-based learning appears in the form of a large (overproduced) repertoire of songs in the plastic phase of song development. During the transition from plastic to crystallized song, social interactions selectively reinforce performance of certain song types, while non-reinforced song types are discarded. We review evidence from three species of sparrow which suggests that song sharing among territorial males, a common form of vocal plasticity usually thought to solely involve memory-based learning, may be the result of action-based learning. These forms of song learning are complementary in that memory-based learning provides the raw song material upon which the selective forces of action-based learning act. We suggest that action-based learning may be widespread among behaviour patterns that involve overproduction of motor patterns in youth.