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Developmental constraints on an adaptive plasticity: reaction norms of pigmentation in adult segments of Drosophila melanogaster.

Variation of dark pigmentation according to developmental temperature was investigated in two geographic populations (France and India) with the isofemale line technique (20 lines for each population). The response curves called the reaction norms, were established in females for seven different segments: the mesothorax and abdomen segments 2-7 (Abd 2-7). In all cases the response curves were non-linear and had to be described either by a quadratic convex polynomial for thorax and Abd 2-5, or by a cubic polynomial for Abd 6 and 7. Among abdomen segments, increasing antero-posterior gradients were observed for several traits, including average pigmentation, overall phenotypic plasticity, the temperature of minimum pigmentation, and the curvature parameter of quadratic norms. Genetic correlations between abdomen segments were high when adjacent segments were considered, but became nil when more distant segments were correlated, suggesting that different pigmentation genes are expressed in the anterior and the posterior part of the abdomen. Characteristic values of reaction norms provided information either on trait value (i.e., the extension of pigmentation) or on plasticity. Correlations between plasticity and pigmentation were generally low and non-significant, suggesting their genetic independence. The overall darker pigmentation which is observed at low temperatures is assumed to be an adaptive plasticity. However, the differences which are evidenced among segments reveal strong interactions with developmental genes. These interactions are less likely to be a consequence of natural selection and are better interpreted as developmental constraints. The reaction norms analysis reveals the complexity of these interactions and should help, in the future, in the identification of the responsible thermosensitive genes.

Adaptation, Physiological↗

PubMed2006

Local and global costs of adaptive plasticity to density in Arabidopsis thaliana.

Although phenotypic plasticity is demonstrably adaptive in a range of settings, organisms are not perfectly plastic. Costs of plasticity comprise one factor predicted to counter the evolution of this adaptive strategy, yet evidence of costs is rare. Here, we test the fitness effects of plastic life-history and morphological responses to density and costs of this plasticity in recombinant inbred lines of Arabidopsis thaliana. Several costs of plasticity and homeostasis were detected. Of particular relevance, there was a significant cost of plasticity to active stem-elongation responses, an adaptive trait in many species. There was also a cost of plasticity to apical branch production at both high and low density, which resulted from the greater suppression of basal branching in genotypes with plastic apical branch production relative to genotypes with fixed apical branch production. The presence of a cost in multiple environments (i.e., a global cost) is predicted to counter the evolution of plasticity. Experimental segregating progenies such as the one used here are expected to have higher genetic costs of plasticity than arrays of genotypes sampled from natural populations because selection should remove genotypes with costs resulting from linkage disequilibrium or epistasis. The use of experimental progeny arrays therefore increases the ability to evaluate genetic costs.

Adaptation, Physiological↗

PubMed2005

Quantitative trait loci affecting delta13C and response to differential water availibility in Arabidopsis thaliana.

Phenotypic plasticity is an important response mechanism of plants to environmental heterogeneity. Here, we explored the genetic basis of plastic responses of Arabidopsis thaliana to water deficit by experimentally mapping quantitative trait loci (QTL) in two recombinant inbred populations (Cvi x Ler and Ler x Col). We detected genetic variation and significant genotype-by-environment interactions for many traits related to water use. We also mapped 26 QTL, including six for carbon isotope composition (delta13C). Negative genetic correlations between fruit length and fruit production as well as between flowering time and branch production were corroborated by QTL colocalization, suggesting these correlations are due to pleiotropy or physical linkage. Water-limited plants were more apically dominant with greater root:shoot ratios and higher delta13C (higher water-use efficiency) when compared to well-watered plants. Many of the QTL effects for these traits interacted significantly with the irrigation treatment, suggesting that the observed phenotypic plasticity is genetically based. We specifically searched for epistatic (QTL-QTL) interactions using a two-dimensional genome scan, which allowed us to detect epistasis regardless of additive genetic effects. We found several significant QTL-QTL interactions including three that exhibited environmental dependence. These results provide preliminary evidence for proposed genetic mechanisms underlying phenotypic plasticity.

Arabidopsis↗

PubMed2026

Context matters: coordinated transcriptional regulation and root plasticity under multinutrient conditions.

Plants often encounter simultaneous imbalances in multiple nutrients, but the regulatory logic coordinating their responses remains poorly understood. We aimed to uncover shared transcriptional programs and regulatory nodes underpinning multinutrient adaptation in Arabidopsis thaliana roots. We analyzed publicly available RNA-seq datasets spanning 15 nutrient and beneficial element conditions using differential expression, co-expression network (WGCNA), and gene regulatory network analysis. Selected transcription factors (TFs) were validated via root phenotyping, suberin staining, and ionomic profiling under two-nutrient stress conditions. We identified a core set of 2050 genes responsive to multiple nutrient treatments, enriched for suberin biosynthesis, and structured into modular co-expression clusters. Eight prioritized candidate TFs (ARR10, GBF3, HHO5, NAC32, NF-YA3, NF-YB2, SARD1, and WRKY33) were shown to modulate root system architecture under specific nutrient combinations. WRKY33 and NF-YB2, in particular, regulated nutrient-responsive suberin deposition and ionomic plasticity. These findings reveal suberin remodeling as a shared downstream process in multinutrient responses and suggest that plasticity is not a fixed trait but a modular, polygenic, and context-dependent outcome. Repurposed TFs with pleiotropic functions coordinate structural and physiological traits, providing regulatory entry points for improving nutrient resilience.

Plant Roots↗

PubMed1995

Plasticity in cultured carotid body chemoreceptors: environmental modulation of GAP-43 and neurofilament.

In this study we use dissociated cell cultures of the rat carotid body to investigate the adaptive capabilities of endogenous oxygen chemoreceptors, following chronic stimulation by various environmental factors. These oxygen chemoreceptors are catecholamine-containing glomus cells, which derive from the neural crest and resemble adrenal medullary chromaffin cells. Using double-label immunofluorescence, we found that chronic exposure of carotid body cultures to hypoxia (2% to 10% oxygen) caused a significant fraction of tyrosine hydroxylase-positive (TH+) glomus cells to acquire detectable immunoreactivity for growth-associated protein GAP-43. The effect was dose-dependent and peaked around an oxygen tension of 6%, where approximately 30% of glomus cells were GAP-43 positive. Treatment with agents that elevate intracellular cyclic adenosine monophosphate (cAMP) (i.e., dibutyryl cAMP or forskolin) also markedly stimulated GAP-43 expression. Since hypoxia is known to increase cAMP levels in glomus cells, it is possible that the effect of hypoxia on GAP-43 expression was mediated, at least in part, by a cAMP-dependent pathway. Unlike hypoxia, however, cAMP analogs also stimulated neurofilament (NF 68 or NF 160 kD) expression and neurite outgrowth in glomus cells, and these properties were enhanced by retinoic acid. Nerve growth factor, which promotes neuronal differentiation in related crest-derived endocrine cells, and dibutyryl cGMP were ineffective. Thus, it appears that postnatal glomus cells are plastic and can express neuronal traits in vitro. However, since hypoxia stimulated GAP-43 expression, without promoting neurite outgrowth, it appears that the two processes can be uncoupled. We suggest that stimulation of GAP-43 by hypoxia may be important for other physiological processes, e.g., enhancing neurotransmitter release or sensitization of G-protein-coupled receptor transduction.

Animals↗

PubMed2002

Experimental life-history evolution: selection on the allocation to sexual reproduction and its plasticity in a clonal plant.

Allocation to sexual reproduction is an important life-history trait in clonal plants. Different selection pressures between competitive and competition-free environments are likely to result in the evolution of specialized genotypes and to maintain genetic variation in reproductive allocation. Moreover, selection may also result in the evolution of plastic allocation strategies. The necessary prerequisite for evolution, heritable genetic variation, can best be studied with selection experiments. Starting from a base population of 102 replicated genotypes of the clonal herb Ranunculus reptans, we imposed selection on the proportion of flowering rosettes in the absence of competition (base population: mean = 0.391, broad-sense heritability = 0.307). We also selected on the plasticity in this trait in response to competition with a naturally coexisting grass in a parallel experiment (base population: 14% lower mean in the presence of competition, broad-sense heritability = 0.072). After two generations of bidirectional selection, the proportion of flowering rosettes was 26% higher in the high line than in the low line (realized heritability +/- SE = 0.205 +/- 0.017). Moreover, genotypes of the high line had 11% fewer carpels per flower, a 22% lower proportion of rooted rosettes, and a 39% smaller average distance between rosettes within a clone. In the second experiment, we found no significant responses to selection for high and low plasticity in the proportion of flowering rosettes (realized heritability +/- SE = -0.002 +/- 0.013). Our study indicates a high heritability and potential for further evolution of the proportion of flowering rosettes in R. reptans, but not for its plasticity, which may have been fixed by past evolution at its current level. Moreover, our results demonstrate strong genetic correlations between allocation to sexual reproduction and other clonal life-history characteristics.

Biological Evolution↗

PubMed2006

Genome-wide scan reveals that genetic variation for transcriptional plasticity in yeast is biased towards multi-copy and dispensable genes.

One of the most important aspects of the evolution of development and physiology is the interplay between gene expression and the environment, by which traits become altered in response to environmental triggers. This feature is known as phenotypic plasticity. When different genotypes show different levels of plasticity for a trait, then they show genotype-by-environment interaction, or GEI. It is now clear that gene expression plays an important role in organismic-level phenotypic plasticity, but we know very little about whether gene expression itself is subject to genetic variation for phenotypic plasticity (GEI). Given that gene regulation is likely to have evolved to respond to environmental changes, it is of central importance to understand how environmental and genetic variation interact to produce variation in gene expression. Here we investigate genetic variation for phenotypic plasticity in the yeast transcriptome for the whole genome. Six strains of Saccharomyces cerevisiae were grown in four different environments representing a continuum of rich and poor natural conditions. Using DNA-microarray data and an ANOVA analysis with a stringent criterion of significance, we found significant genetic variation for transcriptional plasticity (GEI) among strains for approximately 5% of the genes in the genome. There are about twice as many genes that show genetic variation for phenotypic plasticity as show genetic variation in transcription level independent of the environment. We also found that genes with genetic variation for plasticity were less likely to be essential and were significantly biased towards genes that have paralogs.

Adaptation, Physiological↗

PubMed2006

Plasticity of physiology in Lobelia: testing for adaptation and constraint.

Phenotypic plasticity is thought to be a major mechanism allowing sessile organisms such as plants to adapt to environmental heterogeneity. However, the adaptive value of many common plastic responses has not been tested by linking these responses to fitness. Even when plasticity is adaptive, costs of plasticity, such as the energy necessary to maintain regulatory pathways for plastic responses, may constrain its evolution. We used a greenhouse experiment to test whether plastic physiological responses to soil water availability (wet vs. dry conditions) were adaptive and/or costly in the congeneric wildflowers Lobelia cardinalis and L. siphilitica. Eight physiological traits related to carbon and water uptake were measured. Specific leaf area (SLA), photosynthetic rate (A), stomatal conductance (gs), and photosynthetic capacity (Amax) responded plastically to soil water availability in L. cardinalis. Plasticity in Amax was maladaptive, plasticity in A and g(s) was adaptive, and plasticity in SLA was adaptively neutral. The nature of adaptive plasticity in L. cardinalis, however, differed from previous studies. Lobelia cardinalis plants with more conservative water use, characterized by lower g(s), did not have higher fitness under drought conditions. Instead, well-watered L. cardinalis that had higher g(s) had higher fitness. Only Amax responded plastically to drought in L. siphilitica, and this response was adaptively neutral. We detected no costs of plasticity for any physiological trait in either L. cardinalis or L. siphilitica, suggesting that the evolution of plasticity in these traits would not be constrained by costs. Physiological responses to drought in plants are presumed to be adaptive, but our data suggest that much of this plasticity can be adaptively neutral or maladaptive.

Acclimatization↗

PubMed2000

Costs of plasticity in foraging characteristics of the clonal plant Ranunculus reptans.

In clonal plants, evolution of plastic foraging by increased lengths of leaves and internodes under unfavourable conditions may be constrained by costs and limits of plasticity. We studied costs and limits of plasticity in foraging characteristics in 102 genotypes of the stoloniferous herb Ranunculus reptans. We grew three replicates of each genotype with and three without competition by the naturally co-occuring grass Agrostis stolonifera. We used regression and correlation analyses to investigate potential costs of plasticity in lengths of leaves and stolon internodes, developmental instability costs of these traits, and a developmental range limit of these traits. We used randomization procedures to control for spurious correlations between parameters calculated from the same data. Under competition the number of rosettes, rooted rosettes, and flowers was 58%, 40%, and 61% lower, respectively, than in the absence of competition. Under competition lengths of leaves and stolon internodes were 14% and 6% smaller, respectively, than in the absence of competition. We detected significant costs of plasticity in stolon internode length in the presence of competition when fitness was measured in terms of the number of rosettes and the number of flowers (selection gradients against plasticity were 0.250 and 0.214, respectively). Within-environment variation (SD) in both foraging traits was not positively correlated with the corresponding plasticity, which indicates that there were no developmental instability costs. More plastic genotypes did not have less extreme trait values than less plastic genotypes for both foraging traits, which indicates that there was no developmental range limit. We conclude that in R. reptans costs of plasticity more strongly constrain evolution of foraging in the horizontal plane (i.e., stolon internode length) than in the vertical plane (i.e., leaf length).

Adaptation, Physiological↗

PubMed2005

Sonic and electric fish: at the crossroads of neuroethology and behavioral neuroendocrinology.

Field and laboratory studies of weakly electric and sound-producing teleost fishes demonstrate how steroidal and non-steroidal hormones mediate the translation of neural events into behavior. The development of this research program has depended upon an interdisciplinary neuroethological approach that has characterized the neurophysiological properties of the motor and sensory pathways that lead to the production and detection of easily quantified highly stereotyped behaviors, namely, electric organ discharges (EODs) and vocalizations. Neuroethological studies of these teleosts have now integrated a behavioral neuroendocrinology approach that has provided several examples of how hormone-sensitive neurobiological traits contribute to adaptive behavioral plasticity in natural habitats. As such, these studies provide guideposts for comparable studies in other groups of teleosts and vertebrates in general.

Androgens↗

PubMed2005

Genetic and environmental variation in the visual properties of bluefin killifish, Lucania goodei.

Animals use their sensory systems to detect information about the external environment in order to find mates, locate food and habitat and avoid predators. Yet, there is little understanding of the relative amounts of genetic and/or environmental variation in sensory system properties. In this paper, we demonstrate genetic and environmental variation in opsin expression in a population of bluefin killifish. We measured expression of five opsins (which correlates with relative frequency of corresponding cones) using quantitative, real-time polymerase chain reaction for offspring from a breeding study where offspring were raised under different lighting conditions. Sire (i.e. genetic) effects were present for opsin found in yellow photopigment. Dam effects were present for opsins that create violet, blue and red photopigment. Lighting conditions affected expression of all opsins except SWS2A and mimicked the pattern found among populations. These results highlight the fact that sensory systems are both plastic and yet readily evolvable traits.

Analysis of Variance↗

PubMed2001

Developmental and acclimatory contributions to water loss in a desert rodent: investigating the time course of adaptive change.

Understanding the evolution of physiological traits requires considering three nonexclusive mechanisms that underlie phenotypes and cause their change over different time scales: acclimation, developmental plasticity, and natural selection for genetically fixed traits. Physiological adjustments to changes in the desiccating potential of the environment were investigated with one subspecies of common desert rodent, Dipodomys merriami merriami (Merriam's kangaroo rat). We raised young whose parents originated from environments that differ in both temperature and humidity. These young were raised under either desiccating or water-abundant conditions, and their water loss was measured at a series of temperatures to determine the effect developmental conditions have on resistance to desiccation. We then determined the contribution of acclimation to desiccation resistance by keeping the differentially raised young in conditions opposite to those during their development and again measuring water loss. We found that developmental plasticity and acclimation can completely account for the existing intraspecific variability in desiccation resistance under certain conditions. In fact, developmental and acclimatory changes can equal genetically based differences of the populations. This phenotypic plasticity can operate relatively quickly and therefore may attenuate the actions of natural selection. Understanding the extent and nature of such flexibility is critical to our understanding intraspecific variability and the consequences of changing climate.

Acclimatization↗

PubMed2006

Phenotypic plasticity and experimental evolution.

Natural or artificial selection that favors higher values of a particular trait within a given population should engender an evolutionary response that increases the mean value of the trait. For this prediction to hold, the phenotypic variance of the trait must be caused in part by additive effects of alleles segregating in the population, and also the trait must not be too strongly genetically correlated with other traits that are under selection. Another prediction, rarely discussed in the literature, is that directional selection should favor alleles that increase phenotypic plasticity in the direction of selection, where phenotypic plasticity is defined as the ability of one genotype to produce more than one phenotype when exposed to different environments. This prediction has received relatively little empirical attention. Nonetheless, many laboratory experiments impose selection regimes that could allow for the evolution of enhanced plasticity (e.g. desiccation trials with Drosophila that last for several hours or days). We review one example that involved culturing of Drosophila on lemon for multiple generations and then tested for enhanced plasticity of detoxifying enzymes. We also review an example with vertebrates that involves selective breeding for high voluntary activity levels in house mice, targeting wheel-running behavior on days 5+6 of a 6-day wheel exposure. This selection regime allows for the possibility of wheel running itself or subordinate traits that support such running to increase in plasticity over days 1-4 of wheel access. Indeed, some traits, such as the concentration of the glucose transporter GLUT4 in gastrocnemius muscle, do show enhanced plasticity in the selected lines over a 5-6 day period. In several experiments we have housed mice from both the Selected (S) and Control (C) lines with or without wheel access for several weeks to test for differences in plasticity (training effects). A variety of patterns were observed, including no training effects in either S or C mice, similar changes in both the S and C lines, greater changes in the S lines but in the same direction in the C lines, and even opposite directions of change in the S and C lines. For some of the traits that show a greater training effect in the S lines, but in the same direction as in C lines, the greater effect can be explained statistically by the greater wheel running exhibited by S lines ('more pain, more gain'). For others, however, the differences seem to reflect inherently greater plasticity in the S lines (i.e. for a given amount of stimulus, such as wheel running/day, individuals in the S lines show a greater response as compared with individuals in the C lines). We suggest that any selection experiment in which the selective event is more than instantaneous should explore whether plasticity in the appropriate (adaptive) direction has increased as a component of the response to selection.

Adaptation, Physiological↗

PubMed2005

A comparison of phenotypic plasticity in the native dandelion Taraxacum ceratophorum and its invasive congener T. officinale.

We compared plastic responses to variation in the light environment for sympatric populations of native and exotic dandelion species, Taraxacum ceratophorum and Taraxacum officinale. Plasticity in leaf size, inflorescence height, reproductive phenology and dispersal-related traits were measured under experimentally altered light quality (red : far-red light ratio, R : FR) and light intensity (photosynthetically active radiation, PAR). To test whether differences in means and reaction norms of dispersal-related traits between species affected colonization potential, we created seed-dispersal models based on seed-fall rate and release height. Differences in plasticity between species were not systematic, but varied in direction and magnitude among traits. Taraxacum officinale produced larger leaves that exhibited greater plasticity in size under variable light intensity than T. ceratophorum. Plasticity in scape length at flowering occurred in relation to R : FR ratio in both species, but tended to be greater in T. ceratophorum. Seed-bearing scapes of T. officinale were taller and more canalized in height across light regimes than scapes of T. ceratophorum. Seeds of T. officinale were smaller than seeds of T. ceratophorum. Models predict greater dispersal in T. officinale within open and vegetated habitats. In contrast to the idea that plasticity promotes invasiveness, results suggest that the lack of plasticity in dispersal-related traits enhances the colonization potential of T. officinale.

Adaptation, Physiological↗

PubMed2004

Quantitative trait loci affecting growth-related traits in wild barley (Hordeum spontaneum) grown under different levels of nutrient supply.

The genetic basis of phenotypic plasticity of relative growth rate (RGR), its components and associated morphological traits was studied in relation to nutrient limitation. In all, 140 F(3) lines from a cross, made between two Hordeum spontaneum (wild barley) accessions sampled in Israel, were subjected to growth analysis under two nutrient levels. Quantitative trait loci (QTLs) were detected for RGR and three of its components, leaf area ratio (LAR), specific leaf area and leaf mass fraction (LMF). Indications for close linkage (potential pleiotropy) were found, for example, for LAR and LMF. An interesting case is on chromosome 6, at which QTLs for RGR and seed mass were detected in the same region. These QTLs had opposite additive effects, supporting earlier results that plants growing from lighter seeds had a higher RGR. Only two QTLs were significant under both nutrient conditions, suggesting large QTL x environment interactions for most traits. For 21 out of 26 QTLs, however, the additive genetic effect was of identical sign in both nutrient environments, but reached the significance threshold in only one of them. Nevertheless, some QTLs detected in one of the two environments had virtually no effect in the other, and QTLs for plasticity were detected for RGR, LAR and LMF, as well as for some morphological traits. QTLs with opposite effects under high and low nutrients were not found. Thus, at the genetic level, there was no evidence for a trade-off between faster growth at high versus low nutrient levels.

Analysis of Variance↗

PubMed2003

Talkin' 'bout my generation: environmental variability and cohort effects.

In variable environments, it is probable that environmental conditions in the past can influence demographic performance now. Cohort effects occur when these delayed life-history effects are synchronized among groups of individuals in a population. Here we show how plasticity in density-dependent demographic traits throughout the life cycle can lead to cohort effects and that there can be substantial population dynamic consequences of these effects. We show experimentally that density and food conditions early in development can influence subsequent juvenile life-history traits. We also show that conditions early in development can interact with conditions at maturity to shape future adult performance. In fact, conditions such as food availability and density at maturity, like conditions early in development, can generate cohort effects in mature stages. Based on these data, and on current theory about the effects of plasticity generated by historical environments, we make predictions about the consequences of such changes on density-dependent demography and on mite population dynamics. We use a stochastic cohort effects model to generate a range of population dynamics. In accordance with the theory, we find the predicted changes in the strength of density dependence and associated changes in population dynamics and population variability.

Age Factors↗

PubMed2005

Allometry for sexual size dimorphism: testing two hypotheses for Rensch's rule in the water strider Aquarius remigis.

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch's rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch's rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual-selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential-plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are "adaptively canalized." While this hypothesis is unlikely to explain Rensch's rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.

Animals↗

PubMed2025

Complex and Dynamic Gene-by-Age and Gene-by-Environment Interactions Underlie Functional Morphological Variation in Adaptive Divergence in Arctic Charr (Salvelinus alpinus).

The evolution of adaptive phenotypic divergence requires heritable genetic variation. However, it is underappreciated that trait heritability is molded by developmental processes interacting with the environment. We hypothesized that the genetic architecture of divergent functional traits was dependent on age and foraging environment. Thus, we induced plasticity in full-sib families of Arctic charr (Salvelinus alpinus) morphs from two Icelandic lakes by mimicking prey variation in the wild. We characterized variation in body shape and size at two ages and investigated their genetic architecture with quantitative trait locus (QTL) analysis. Age had a greater effect on body shape than diet in most families, suggesting that development strongly influences phenotypic variation available for selection. Consistent with our hypothesis, multiple QTL were detected for all traits and their location depended on age and diet. Many of the genome-wide QTL were located within a subset of duplicated chromosomal regions suggesting that ancestral whole genome duplication events have played a role in the genetic control of functional morphological variation in the species. Moreover, the detection of two body shape QTL after controlling for the effects of age provides additional evidence for genetic variation in the plastic response of morphological traits to environmental variation. Thus, functional morphological traits involved in phenotypic divergence are molded by complex genetic interactions with development and environment.

Animals↗