Phenotypic plasticity for life-history traits in Drosophila melanogaster. III. Effect of the environment on genetic parameters.

We estimated genetic and environmental variance components for developmental time and dry weight at eclosion in Drosophila melanogaster raised in ten different environments (all combinations of 22, 25 and 28 degrees C and 0.5, 1 and 4% yeast concentration, and 0.25% yeast at 25 degrees C). We used six homozygous lines derived from a natural population for complete diallel crosses in each environment. Additive genetic variances were consistently low for both traits (h2 around 10%). The additive genetic variance of developmental time was larger at lower yeast concentrations, but the heritability did not increase because other components were also larger. The additive genetic effects of the six parental lines changed ranks across environments, suggesting a mechanism for the maintenance of genetic variation in heterogenous environments. The variance due to non-directional dominance was small in most environments. However, there was directional dominance in the form of inbreeding depression for both traits. It was pronounced at high yeast levels and temperatures but disappeared when yeast or temperature were decreased. This meant that the heterozygous flies were more sensitive to environmental differences than homozygous flies. Because dominance effects are not heritable, this suggests that the evolution of plasticity can be constrained when dominance effects are important as a mechanism for plasticity.     

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

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

Evolution and maintenance of the environmental component of the phenotypic variance: benefit of plastic traits under changing environments

How environmental variances in quantitative traits are influenced by variable environments is an important problem in evolutionary biology. In this study, the evolution and maintenance of phenotypic variance in a plastic trait under stabilizing selection are investigated. The mapping from genotypic value to phenotypic value of the quantitative trait is approximated by a linear reaction norm, with genotypic effects on its phenotypic mean and sensitivity to environment. The environmental deviation is assumed to be decomposed into environmental quality, which interacts with genotypic value, and residual developmental noise, which is independent of genotype. Environmental quality and the optimal phenotype of stabilizing selection are allowed to randomly fluctuate in both space and time, and individuals migrate equally before development and reproduction among different niches. Analyses show that phenotypic plasticity is adaptive within variable environments if correlations have become established between the optimal phenotype and environmental quality in space and/or time. The evolved plasticity increases with variances in optimal phenotypes and correlations between optimal phenotype and environmental quality; this further induces increases in mean fitness and the environmental variance in the trait. Under certain circumstances, however, the environmental variance may decrease with increase in variation in environmental quality.     

Behaviour-genetic analysis of Phormia regina II. Detection of a single,major-gene effect from behavioural variation for Central Excitatory State (CES) using hybrid crosses

Converging evidence from replicated hybrid analyses (and from selection and single-pair mating; Tully & Hirsch 1982) points to a single, major-gene correlate of the central excitatory state (CES) in pure breeding lines of the black blow-fly, Phormia regina. Analysis of reciprocal F₁s reveals no X-chromosome or cytoplasmic effects. Biometrical analysis indicates significant additive and environmental phenotypic variance components. No net dominance deviation or dominance variance is detectable (which is consistent with absence of intralocular dominance). An estimate of the number of segregating loci is near 1. A more general non-parametric method fails to reject the one-gene model.     

The Genetics of Copper Tolerance in the Yellow Monkey Flower, MIMULUS GUTTATUS. I. Crosses to Nontolerants

The biometrical genetics of copper tolerance has been investigated in two Californian populations of Mimulus guttatus by crosses to a nontolerant British population. A simple biometrical model involving only additive and dominance effects is not sufficient. When the first order interactions are included, the model is shown to fit the data. Interactions between the dominance effects of different loci, and between dominance and additive effects, are the most important. These interactions can be explained either by a threshold model, or by postulating dominance modification.     

Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments

Adaptive plasticity is expected to be important when the grain of environmental variation is encompassed in offspring dispersal distance. We investigated patterns of local adaptation, selection and plasticity in an association of plant morphology with fine-scale habitat shifts from oak canopy understory to adjacent grassland habitat in Claytonia perfoliata. Populations from beneath the canopy of oak trees were >90 % broad leaved and large seeded, while plants from adjacent grassland habitat were >90 % linear-leaved and small seeded. In a 2-year study, we used reciprocal transplants and phenotypic selection analysis to investigate local adaptation, selection, plasticity and maternal effects in this trait-environment association. Transgenerational effects were studied by planting offspring of inbred maternal families grown in both environments across the same environments in the second year. Reciprocal transplants revealed local adaptation to habitat type: broad-leaved forms had higher fitness in oak understory and linear-leaved plants had higher fitness in open grassland habitat. Phenotypic selection analyses indicated selection for narrower leaves and lower SLA in open habitat, and selection for broad leaves and intermediate values of SLA in understory. Both plant morphs exhibited plastic responses in traits in the same direction as selection on traits (narrower leaves and lower SLA in open habitat) suggesting that plasticity is adaptive. We detected an adaptive transgenerational effect in which maternal environment influenced offspring fitness; offspring of grassland-reared plants had higher fitness than understory-reared plants when grown in grassland. We did not detect costs of plasticity, but did find a positive association between leaf shape plasticity and fitness in linear-leaved plants in grassland habitat. Together, these findings indicate that fixed differences in trait values corresponding to selection across habitat contribute to local adaptation, but that plasticity and maternal environmental effects may be favored through promotion of survival across heterogeneous environments.     

Signal reliability compromised by genotype-by-environment interaction and potential mechanisms for its preservation

Sexual selection based on signaling requires that signals used by females in mate choice are reliable indicators of a male's heritable total fitness. A signal and the preference for it are expected to be heritable, resulting in the maintenance of genetic covariance between these two traits. However, a recent article has proposed that signals may quickly become unreliable in the presence of both environmental variation and genotype-by-environment interaction (G x E) with crossing reaction norms, potentially compromising the mechanisms of sexual selection. Here we examine the heritability and plasticity of a male dominance advertisement in the bank vole, Clethrionomys glareolus, in stable and changing rearing environments from father to son. The bank vole is naturally exposed to considerable sources of spatial and temporal environmental variation and male reproductive success is determined by both intra- (male-male competition) and inter- (females prefer to mate with dominant males) sexual selection. Significant G x E for male dominance was found with crossing reaction norms. Plasma testosterone level (T), rather than condition, determined a male's dominance and T also showed a significant G x E. Dominance showed a considerable plasticity across environments, but was only heritable under stable conditions. We document a negative between-environments correlation of male dominance, suggesting that when the environment changes between father and son, the dominance signal is unreliable to females and sexual selection may be compromised. We discuss how G x E and environmental variation interacting with other mechanisms may preserve the reliability of signals and thus the mechanism of sexual selection itself.     

The genetics of phenotypic plasticity I. Heritability

Methods for estimating the genetic component of phenotypic plasticity are presented. In the general case of clonal replicates or full-sibs raised in several environments, the heritability of plasticity can be measured as the ratio of the genotype-environment interaction variance to the total phenotypic variance. In the special case of only two environments plasticity also can be measured as the difference among environments in genotype or family means. In that case, the heritability of plasticity can be measured as either a ratio of variance components or as the slope of a parent-offspring regression. The general measure suffers because no least-square standard errors have been developed, although they can be calculated by maximum-likelihood or bootstrapping techniques. For the other two methods least-square standard errors can be calculated but require very large experiments for statistical significance to be achieved. The heritability measures are compared using data on plasticity of thorax size in response to temperature in Drosophila melanogaster. The heritability estimates are all in close agreement. Models of the evolution of phenotypic plasticity have treated it as a trait in its own right and as a cross-environment genetic correlation. Although the first approach is the one used here, neither one is preferred.     

Genetic Variation in a Heterogeneous Environment. II. Temporal Heterogeneity and Directional Selection

The maintenance of genetic variation is investigated in a finite population where selection at an autosomal locus with two alleles varies temporally between two environments and the heterozygote has an intermediate fitness value. When there is additive gene action and equal selection in both environments, the autocorrelation between subsequent environments must be negative for more maintenance of genetic variation than for neutrality. The maximum maintenance occurs when there is equal selection in the two environments and the autocorrelation approaches ^-1.0 (for a stochastic model), or when there is short repeating cycle such as one related to seasons. Also comparison of the effects of stochastic variation in selection in finite and infinite populations is made by using Monte Carlo simulation. One situation was found where temporal environmental variation maintains genetic variation very effectively even in a small population and that is when there is evolution of dominance, i.e., the heterozygote is closer in fitness to the favored homozygote than the other homozygote. An important conclusion is that in a finite population genetic tracing of environmental change, particularly when there is a positive autocorrelation between environments or a long environmental cycle, leads to an increased loss of genetic variation making such a response undesirable in the long term, a result different from that in infinite populations.     

Genotype by environment interaction for adult body weights of shrimp Penaeus vannamei when grown at low and high densitie

Shrimp is one of few marine species cultured worldwide for which several selective breeding programs are being conducted. One environmental factor that can affect the response to selection in breeding programs is the density at which the shrimp are cultured (low-medium-high). Phenotypic plasticity in the growth response to different densities might be accompanied by a significant genotype by environment interaction, evidenced by a change in heritabilities between environments and by a genetic correlation less than one for a unique trait between environments. Our goal was to understand whether different growth densities affect estimates of those genetic parameters for adult body weight (BW) in the Pacific white shrimp (Penaeus vannamei). BW heritabilities were significantly different between environments, with the largest at high density. These differences resulted from both an increased additive genetic variance and a decreased environmental variance when grown at high density. The genetic correlation between BWs at the two environmental conditions was significantly less than one. Whereas these results might be suggestive for carrying out shrimp selective breeding for BW under high density conditions, further understanding of genetic correlations between growth and reproductive traits within a given environment is necessary, as there are indications of reduced reproductive fitness for shrimp grown at high densities.     

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

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

The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics

We model the evolution of reaction norms focusing on three aspects: frequency-dependent selection arising from resource competition, maintenance and production costs of phenotypic plasticity, and three characteristics of environmental heterogeneity (frequency of environments, their intrinsic carrying capacity and the sensitivity to phenotypic maladaptation in these environments). We show that (i) reaction norms evolve so as to trade adaptation for acquiring resources against cost avoidance; (ii) maintenance costs cause reaction norms to better adapt to frequent rather than to infrequent environments, whereas production costs do not; and (iii) evolved reaction norms confer better adaptation to environments with low rather than with high intrinsic carrying capacity. The two previous findings contradict earlier theoretical results and originate from two previously unexplored features that are included in our model. First, production costs of phenotypic plasticity are only incurred when a given phenotype is actually produced. Therefore, they are proportional to the frequency of environments, and these frequencies thus affect the selection pressure to avoid costs just as much as the selection pressure to improve adaptation. This prevents the frequency of environments from affecting the evolving reaction norm. Secondly, our model describes the evolution of plasticity for a phenotype determining an individual's capability to acquire resources, and thus its realized carrying capacity. When individuals are distributed randomly across environments, they cannot avoid experiencing environments with intrinsically low carrying capacity. As selection pressures arising from the need to improve adaptation are stronger under such extreme conditions than under mild ones, better adaptation to environments with low rather than with high intrinsic carrying capacity results.     

Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses

Phenotypic plasticity is a key factor for the success of organisms in heterogeneous environments. Although many forms of phenotypic plasticity can be induced and retracted repeatedly, few extant models have analyzed conditions for the evolution of reversible plasticity. We present a general model of reversible plasticity to examine how plastic shifts in the mode and breadth of environmental tolerance functions (that determine relative fitness) depend on time lags in response to environmental change, the pattern of individual exposure to inducing and noninducing environments, and the quality of available information about the environment. We couched the model in terms of prey-induced responses to variable predation regimes. With longer response lags relative to the rate of environmental change, the modes of tolerance functions in both the presence or absence of predators converge on a generalist strategy that lies intermediate between the optimal functions for the two environments in the absence of response lags. Incomplete information about the level of predation risk in inducing environments causes prey to have broader tolerance functions even at the cost of reduced maximal fitness. We give a detailed analysis of how these factors and interactions among them select for joint patterns of mode and breadth plasticity.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. III. PHENOTYPIC PLASTICITY AND THE MAINTENANCE OF GENETIC VARIATION

Cheilostome bryozoan species show long-term morphologic stasis, implying stabilizing selection sustained for millions of years, but nevertheless retain significant heritable variation in traits of skeletal morphology. The possible role of within-genotype (within-colony) phenotypic variability in preserving genetic diversity was analyzed using breeding data for two species of Stylopoma from sites along 110 km of the Caribbean coast of Panama. Variation among zooids within colonies accounts for nearly two-thirds of the phenotypic variance on average, increases with environmental heterogeneity, and includes significant genotype-environment interaction. Thus, within-colony variability apparently represents phenotypic plasticity, at least some of which is heritable, rather than random “developmental noise.” Almost all of the among-colonies component of phenotypic variance is accounted for by additive genetic differences in trait means, suggesting that within-colony plasticity includes virtually all of the environmental component of phenotypic variance in these populations of Stylopoma. Thus, heritable within-colony plasticity could play a significant part in maintaining genetic diversity in cheilostomes, but it is also possible that rates of polygenic mutation alone are sufficient to balance the effects of selection.     

Multivariate selection shapes environment-dependent variation in the clonal morphology of a red seaweed

Within-individual strategies of variation (e.g., phenotypic plasticity) are particularly relevant to modular organisms, in which ramets of the same genetic individual may encounter diverse environments imposing diverse patterns of selection. Hence, measuring selection in heterogeneous environments is essential to understanding whether environment-dependent phenotypic change enhances the fitness of modular individuals. In sublittoral marine habitats, competition for light and space among modular taxa generates extreme patchiness in resource availability. Little is known, however, of the potential for plasticity within individuals to arise from spatially-variable selection in such systems. We tested whether plasticity enhances genet-level fitness in Asparagopsis armata, a clonal seaweed in which correlated traits mediate morphological responses to variation in light. Using the capacity for rapid, clonal growth to measure fitness, we identified aspects of ramet morphology targeted by selection in two contrasting light environments and compared patterns of selection across environments. We found that directional selection on single traits, coupled with linear and nonlinear selection on multi-trait interactions, shape ramet morphology within environments and favor different phenotypes in each. Evidence of environment-dependent, multivariate selection on correlated traits is novel for any marine modular organism and demonstrates that seaweeds, such as A. armata, may potentially adapt to environmental heterogeneity via plasticity in clonal morphology.     

The consequences of including non-additive effects on the genetic evaluation of harvest body weight in Coho salmon (Oncorhynchus kisutch)

Background

In this study, we used different animal models to estimate genetic and environmental variance components on harvest weight in two populations of Oncorhynchus kisutch, forming two classes i.e. odd- and even-year spawners.

Methods

The models used were: additive, with and without inbreeding as a covariable (A + F and A respectively); additive plus common environmental due to full-sib families and inbreeding (A + C + F); additive plus parental dominance and inbreeding (A + D + F); and a full model (A + C + D + F). Genetic parameters and breeding values obtained by different models were compared to evaluate the consequences of including non-additive effects on genetic evaluation.

Results

Including inbreeding as a covariable did not affect the estimation of genetic parameters, but heritability was reduced when dominance or common environmental effects were included. A high heritability for harvest weight was estimated in both populations (even = 0.46 and odd = 0.50) when simple additive models (A + F and A) were used. Heritabilities decreased to 0.21 (even) and 0.37 (odd) when the full model was used (A + C + D + F). In this full model, the magnitude of the dominance variance was 0.19 (even) and 0.06 (odd), while the magnitude of the common environmental effect was lower than 0.01 in both populations. The correlation between breeding values estimated with different models was very high in all cases (i.e. higher than 0.98). However, ranking of the 30 best males and the 100 best females per generation changed when a high dominance variance was estimated, as was the case in one of the two populations (even).

Conclusions

Dominance and common environmental variance may be important components of variance in harvest weight in O. kisutch, thus not including them may produce an overestimation of the predicted response; furthermore, genetic evaluation was seen to be partially affected, since the ranking of selected animals changed with the inclusion of non-additive effects in the animal model.     

Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments

Adaptive phenotypic plasticity evolves when cues reliably predict fitness consequences of life‐history decisions, whereas bet hedging evolves when environments are unpredictable. These modes of response should be jointly expressed, because environmental variance is composed of both predictable and unpredictable components. However, little attention has been paid to the joint expression of plasticity and bet hedging. Here, I examine the simultaneous expression of plasticity in germination rate and two potential bet‐hedging traits – germination fraction and within‐season diversification in timing of germination – in seeds from multiple seed families of five geographically distant populations of Lobelia inflata (L.) subjected to a thermal gradient. Populations differ in germination plasticity to temperature, in total germination fraction and in the expression of potential diversification in the timing of germination. The observation of a negative partial correlation between the expression of plasticity and germination variance (potential diversification), and a positive correlation between plasticity and germination fraction is suggestive of a trade‐off between modes of response to environmental variance. If the observed correlations are indicative of those between adaptive plasticity and bet hedging, we expect an optimal balance to exist and differ among populations. I discuss the challenges involved in testing whether the balance between plasticity and bet hedging depends on the relative predictability of environmental variance.     

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation,population viability and genetic variation

An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.     

Unifying Genetic Canalization,Genetic Constraint,and Genotype-by-Environment Interaction: QTL by Genomic Background by Environment Interaction of Flowering Time in Boechera stricta

Natural populations exhibit substantial variation in quantitative traits. A quantitative trait is typically defined by its mean and variance, and to date most genetic mapping studies focus on loci altering trait means but not (co)variances. For single traits, the control of trait variance across genetic backgrounds is referred to as genetic canalization. With multiple traits, the genetic covariance among different traits in the same environment indicates the magnitude of potential genetic constraint, while genotype-by-environment interaction (GxE) concerns the same trait across different environments. While some have suggested that these three attributes of quantitative traits are different views of similar concepts, it is not yet clear, however, whether they have the same underlying genetic mechanism. Here, we detect quantitative trait loci (QTL) influencing the (co)variance of phenological traits in six distinct environments in Boechera stricta, a close relative of Arabidopsis. We identified nFT as the QTL altering the magnitude of phenological trait canalization, genetic constraint, and GxE. Both the magnitude and direction of nFT''s canalization effects depend on the environment, and to our knowledge, this reversibility of canalization across environments has not been reported previously. nFT''s effects on trait covariance structure (genetic constraint and GxE) likely result from the variable and reversible canalization effects across different traits and environments, which can be explained by the interaction among nFT, genomic backgrounds, and environmental stimuli. This view is supported by experiments demonstrating significant nFT by genomic background epistatic interactions affecting phenological traits and expression of the candidate gene, FT. In contrast to the well-known canalization gene Hsp90, the case of nFT may exemplify an alternative mechanism: Our results suggest that (at least in traits with major signal integrators such as flowering time) genetic canalization, genetic constraint, and GxE may have related genetic mechanisms resulting from interactions among major QTL, genomic backgrounds, and environments.