The genetics of phenotypic plasticity. III. Genetic correlations and fluctuating asymmetries

We examined the relationship of three aspects of development, phenotypic plasticity, genetic correlations among traits, and developmental noise, for thorax length, wing length, and number of sternopleural bristles in Drosophila melanogaster. We used 14 lines which had previously been selected on either thorax length or plasticity of thorax length in response to temperature. A half-sib mating design was used and offspring were raised at 19° C or 25° C. We found that genetic correlations were stable across temperatures despite the large levels of plasticity of these traits. Plasticities were correlated among developmentally related traits, thorax and wing length, but not among unrelated traits, lengths and bristle counts. Amount of developmental noise, measured as fluctuating asymmetry and within-environmental variation, was positively correlated with amount of plasticity only for some traits, thorax length and bristle number, and only at one temperature, 25° C.     

LATITUDINAL VARIATION OF WING:THORAX SIZE RATIO AND WING-ASPECT RATIO IN DROSOPHILA MELANOGASTER

In dipterans, the wing-beat frequency, and, hence, the lift generated, increases linearly with ambient temperature. If flight performance is an important target of natural selection, higher wing:thorax size ratio and wing-aspect ratio should be favored at low temperatures because they increase the lift for a given body weight. We investigated this hypothesis by examining wing: thorax size ratio and wing-aspect ratio in Drosophila melanogaster collected from wild populations along a latitudinal gradient and in their descendants reared under standard laboratory conditions. In a subset of lines, we also studied the phenotypic plasticity of these traits in response to temperature. To examine whether the latitudinal trends in wing:thorax size ratio and wing-aspect ratio could have resulted from a correlated response to latitudinal selection on wing area, we investigated the correlated responses of these characters in lines artificially selected for wing area. In both the geographic and the artificially selected lines, wing:thorax size ratio and wing-aspect ratio decreased in response to increasing temperature during development. Phenotypic plasticity for either trait did not vary among latitudinal lines or selective regimes. Wing:thorax size ratio and wing-aspect ratio increased significantly with latitude in field-collected flies. The cline in wing:thorax size ratio had a genetic component, but the cline in wing-aspect ratio did not. Artificial selection for increased wing area led to a statistically insignificant correlated increase in wing:thorax size ratio and a decrease in wing-aspect ratio. Our observations are consistent with the hypotheses that high wing-thorax size ratio and wing aspect ratio are per se selectively advantageous at low temperatures.     

Quantitative Genetics of DROSOPHILA MELANOGASTER. I. Sexual Dimorphism in Genetic Parameters for Wing Traits

Sexual dimorphism in genetic parameters is examined for wing dimensions of Drosophila melanogaster. Data are fit to a quantitative genetic model where phenotypic variance is a linear function of additive genetic autosomal variance (common to both sexes), additive genetic X-linked variances distinct for each sex, variance due to common rearing environment of families, residual environmental variance, random error variance due to replication, and variance due to measurement error and developmental asymmetry (left vs. right sides). Polygenic dosage compensation and its effect on genetic variances and covariances between sexes is discussed. Variance estimates for wing length and other wing dimensions highly correlated with length support the hypothesis that the Drosophila system of dosage compensation will cause male X-linked genetic variance to be substantially larger than female X-linked variance. Results for various wing dimensions differ, suggesting that the level of dosage compensation may differ for different traits. Genetic correlations between sexes for the same trait are presented. Total additive genetic correlations are near unity for most wing traits; this indicates that selection in the same direction in both sexes would have a minor effect on changing the magnitude of difference between sexes. Additive X-linked correlations suggest some genotype x sex interactions for X-linked effects.     

Study of Natural Genetic Variation in Early Fitness Traits Reveals Decoupling Between Larval and Pupal Developmental Time in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Characterizing the relationships between genotype and phenotype for developmental adaptive traits is essential to understand the evolutionary dynamics underlying biodiversity. In holometabolous insects, the time to reach the reproductive stage and pupation site preference are two such traits. Here we characterize aspects of the genetic architecture for Developmental Time (decomposed in Larval and Pupal components) and Pupation Height using lines derived from three natural populations of Drosophila melanogaster raised at two temperatures. For all traits, phenotypic differences and variation in plasticity between populations suggest adaptation to the original thermal regimes. However, high variability within populations shows that selection does not exhaust genetic variance for these traits. This could be partly explained by local adaptation, environmental heterogeneity and modifications in the genetic architecture of traits according to environment and ontogenetic stage. Indeed, our results show that the genetic factors affecting Developmental Time and Pupation Height are temperature-specific. Varying relationships between Larval and Pupal Developmental Time between and within populations also suggest stage-specific modifications of genetic architecture for this trait. This flexibility would allow for a somewhat independent evolution of adaptive traits at different environments and life stages, favoring the maintenance of genetic variability and thus sustaining the traits’ evolvabilities.     

High efficiency of a double-screening method on single P-element insertion lines to identify quantitative trait mutants in Drosophila melanogaster

Enhancer trap P-element insertion has become a common method for generating new mutations in Drosophila melanogaster. When this method is used to isolate mutants for quantitative traits, an appropriate control must be established to define normal and mutant phenotypes. Considering that enhancer-trap lines are generated by crossing several strains, usually with no homogeneous genetic background, no clear control strain can be selected. Previous reports tried to overcome this problem by homogenizing the genetic background of the original lines. However, this is not the most common scenario, especially when functional phenotypes are studied in previously generated lines. Without such caution, is it possible to identify functional mutants among P-element insertion lines? We tested this for olfactory preference, a quantitative trait. Using as control measurement the average phenotype of 30 simultaneously generated P-element insertion lines with preferential reporter-gene expression in olfactory reception organs, we found that 25 of the lines exhibited mutant phenotypes in response to one or several of 5 tested odorants. Additional tests showed that the efficiency of the method for detecting olfactory mutations exceeded 60% even for such a small number of tested odorants. According to these results this approach greatly facilitates the identification of putative abnormal phenotypes, which must be extensively confirmed afterwards.     

Evolutionary changes of nonlinear reaction norms according to thermal adaptation: a comparison of two Drosophila species

While the adaptive significance of discontinuous reaction norms is generally accepted, the evolutionary interpretation of continuous response curves remains speculative, and the occurrence of internal constraints is often suggested as an explanation of experimental observations. In Drosophila melanogaster, various morphometrical traits exhibit convex reaction norms to growth temperature, with a maximum value within the developmental thermal range. We compared a cold-adapted species (D. subobscura) with a mid thermal range at 16 °C, to the warm-adapted D. melanogaster (mid thermal range at 22 °C) for three different morphometrical traits: wing and thorax length in both sexes and ovariole number in females. Maximum value temperatures were ordered in the same way for the three traits in both species: ovariole number > thorax length > wing length. Significant differences were also observed between the two species for the curvature parameter of the quadratic adjustment. The major observation was a significant lateral shift in the reaction norms: maximum values were observed at much lower temperatures in the cold-adapted species than in the warm-adapted one. The parallelism between mid thermal range variation and the position of the maximum value strongly suggests an adaptive displacement of the response curves. Natural selection may thus act not only on trait mean values but also on phenotypic plasticity and on the shape of reaction norms.     

Phenotypic plasticity in morphological traits in two populations of Drosophila melanogaster

Isofemale lines of two populations of Drosophila melanogaster, originating from France and Tanzania, were examined over a range of temperatures. Morphological traits showed distinct patterns in phenotypic plasticity; flies of the two populations differed in shape. Genotype-by-Environment (G*E) interactions were frequently found in the Tanzania population, but were hardly present in the France population. If G*E interaction was present over temperature, estimates of additive genetic variance and additive genetic covariance were made to compare theoretical models with our data. The conclusion is that in France Drosophila melanogaster has been selected over a wider range of temperatures, resulting in parallel reaction norms of more optimal slope. In contrast, selection must have taken place over a narrower temperature range in Tanzanian flies, and will have exerted no direct influence on the slope of the reaction norm.     

FITNESS SENSITIVITY AND THE CANALIZATION OF LIFE-HISTORY TRAITS

Canalization is an abstract term that describes unknown developmental mechanisms that reduce phenotypic variation. A trait can be canalized against environmental perturbations (e.g., changes in temperature or nutrient quality), or genetic perturbations (e.g., mutations or recombination); this paper is about genetic canalization. Stabilizing selection should improve the canalization of traits, and the degree of canalization should be positively correlated with the traits' impact on fitness. Experiments testing this idea should measure the canalization of a series of traits whose impact on fitness is known or can be inferred, exclude differences among traits in the number of loci and alleles segregating as an explanation for the pattern of variability found, and distinguish between canalization against genetic and environmental variation. These conditions were met by three experiments within which the variation of fitness components among Drosophila melanogaster lines was measured and among which the genetic contribution to the variation among lines was clearly different. The canalization of the traits increased with their impact on fitness and did not depend on the degree of genetic differences among lines. That the flies used had been transformed by a P-element insert suggests that canalization was also effective against novel genetic variation. The results reported here cannot be explained by the classical hypothesis of reduction in the number of loci segregating for traits with greater impact on fitness and confirm that traits with greater impact on fitness are more strongly canalized. This pattern of canalization reveals an underappreciated role for development in microevolution. There is differential genetic canalization of fitness components in D. melanogaster.     

Novel genetic capacitors and potentiators for the natural genetic variation of sensory bristles and their trait specificity in Drosophila melanogaster

Cryptic genetic variation (CGV) is defined as the genetic variation that has little effect on phenotypic variation under a normal condition, but contributes to heritable variation under environmental or genetic perturbations. Genetic buffering systems that suppress the expression of CGV and store it in a population are called genetic capacitors, and the opposite systems are called genetic potentiators. One of the best‐known candidates for a genetic capacitor and potentiator is the molecular chaperone protein, HSP90, and one of its characteristics is that it affects the genetic variation in various morphological traits. However, it remains unclear whether the wide‐ranging effects of HSP90 on a broad range of traits are a general feature of genetic capacitors and potentiators. In the current study, I searched for novel genetic capacitors and potentiators for quantitative bristle traits of Drosophila melanogaster and then investigated the trait specificity of their genetic buffering effect. Three bristle traits of D. melanogaster were used as the target traits, and the genomic regions with genetic buffering effects were screened using the 61 genomic deficiencies examined previously for genetic buffering effects in wing shape. As a result, four and six deficiencies with significant effects on increasing and decreasing the broad‐sense heritability of the bristle traits were identified, respectively. Of the 18 deficiencies with significant effects detected in the current study and/or by the previous study, 14 showed trait‐specific effects, and four affected the genetic buffering of both bristle traits and wing shape. This suggests that most genetic capacitors and potentiators exert trait‐specific effects, but that general capacitors and potentiators with effects on multiple traits also exist.     

Plant resource-use strategies: the importance of phenotypic plasticity in response to a productivity gradient for two subalpine species

Background and Aims

Functional traits are indicators of plant interactions with their environment and the resource-use strategies of species can be defined through some key functional traits. The importance of genetic variability and phenotypic plasticity in trait variations in response to a common environmental change was investigated in two subalpine species.

Methods

Two species with contrasted resource-use strategies, Dactylis glomerata and Festuca paniculata, were grown along a productivity gradient in a greenhouse experiment. Functional traits of different genotypes were measured to estimate the relative roles of phenotypic plasticity and genetic variability, and to compare their levels of phenotypic plasticity.

Key Results

Trait variability in the field for the two species is more likely to be the result of phenotypic plasticity rather than of genetic differentiation between populations. The exploitative species D. glomerata expressed an overall higher level of phenotypic plasticity compared with the conservative species F. paniculata. In addition to different amplitudes of phenotypic plasticity, the two species differed in their pattern of response for three functional traits relevant to resource use (specific leaf area, leaf dry matter content and leaf nitrogen content).

Conclusions

Functional trait variability was mainly the result of phenotypic plasticity, with the exploitative species showing greater variability. In addition to average trait values, two species with different resource-use strategies differed in their plastic responses to productivity.     

Micro‐geographical scale variation in Drosophila melanogaster larval olfactory behaviour is associated with host fruit heterogeneity

Organisms utilize environmental cues to deal with heterogeneous environments. In this sense, behaviours that mediate interactions between organisms and their environment are complex traits, especially sensitive to environmental conditions. In animals, olfaction is a critical sensory system that allows them to acquire chemical information from the environment. The genetic basis and physiological mechanisms of the olfactory system of Drosophila melanogaster Meigen (Diptera: Drosophilidae) are well known, but the effects of ecological factors on the olfactory system have received less attention. In this study, we analysed the effect of environmental heterogeneity (different host fruits) on variation in larval olfactory behaviour in a natural population of D. melanogaster. We generated half‐sib lines of D. melanogaster derived from two nearby fruit plantations, Vitis vinifera L. (Vitaceae) (‘grape’) and Prunus persica L. (Rosaceae) (‘peach’), and measured, using a simple behavioural assay, larval olfactory response to natural olfactory stimuli. Results indicate that patterns of variation for this trait depend on host fruit plantation where lines were collected. In fact, only lines derived from ‘grape’ showed phenotypic plasticity for larval olfaction, whereas a genotype*environment interaction was detected solely in lines derived from ‘peach’. Therefore, our results demonstrate the existence of genetic differences in D. melanogaster larval olfactory behaviour at a micro‐geographical scale and also reveal that the trait studied presents a dynamic genetic architecture which is strongly influenced by the environment.     

Genetic Architecture of Abdominal Pigmentation in Drosophila melanogaster

Pigmentation varies within and between species and is often adaptive. The amount of pigmentation on the abdomen of Drosophila melanogaster is a relatively simple morphological trait, which serves as a model for mapping the genetic basis of variation in complex phenotypes. Here, we assessed natural variation in female abdominal pigmentation in 175 sequenced inbred lines of the Drosophila melanogaster Genetic Reference Panel, derived from the Raleigh, NC population. We quantified the proportion of melanization on the two most posterior abdominal segments, tergites 5 and 6 (T5, T6). We found significant genetic variation in the proportion of melanization and high broad-sense heritabilities for each tergite. Genome-wide association studies identified over 150 DNA variants associated with the proportion of melanization on T5 (84), T6 (34), and the difference between T5 and T6 (35). Several of the top variants associated with variation in pigmentation are in tan, ebony, and bric-a-brac1, genes known to affect D. melanogaster abdominal pigmentation. Mutational analyses and targeted RNAi-knockdown showed that 17 out of 28 (61%) novel candidate genes implicated by the genome-wide association study affected abdominal pigmentation. Several of these genes are involved in developmental and regulatory pathways, chitin production, cuticle structure, and vesicle formation and transport. These findings show that genetic variation may affect multiple steps in pathways involved in tergite development and melanization. Variation in these novel candidates may serve as targets for adaptive evolution and sexual selection in D. melanogaster.     

REML estimates of genetic parameters of sexual dimorphism for wing and thorax length in<Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Restricted maximum likelihood was used to estimate genetic parameters of male and female wing and thorax length in isofemale lines ofDrosophila melanogaster, and results compared to estimates obtained earlier with the classical analysis of variance approach. As parents within an isofemale line were unknown, a total of 500 parental pedigrees were simulated and mean estimates computed. Full and half sibs were distinguished, in contrast to usual isofemale studies in which animals were all treated as half sibs and hence heritability was overestimated. Heritability was thus estimated at 0.33, 0.38, 0.30 and 0.33 for male and female wing length and male and female thorax length, respectively, whereas corresponding estimates obtained using analysis of variance were 0.46, 0.54, 0.35 and 0.38. Genetic correlations between male and female traits were 0.85 and 0.62 for wing and thorax length, respectively. Sexual dimorphism and the ratio of female to male traits were moderately heritable (0.30 and 0.23 for wing length, 0.38 and 0.23 for thorax length). Both were moderately and positively correlated with female traits, and weakly and negatively correlated with male traits. Such heritabilities confirmed that sexual dimorphism might be a fast evolving trait inDrosophila. An erratum to this article is available at .     

Evolutionary responses of Drosophila melanogaster to selection at different larval densities: changes in genetic variation,specialization and phenotypic plasticity

Abstract We studied the evolutionary response to novel environments by applying artificial selection for total progeny biomass in populations of Drosophila melanogaster maintained at three different larval population densities. We found the relative amount of genetic variability for characters related with biomass to be lower and the correlation between them more negative at the intermediate density, and that selection resulted in changes in phenotypic plasticity and in patterns of resource allocation between traits. We found some evidence for tradeoffs between densities, which suggests that populations living at heterogeneous densities might be subject to disruptive selection. Our results show that adaptation to new environments may be a complex process, involving not only changes in trait means, but also in correlations between traits and between environments.     

Stage-Specific Effects of Candidate Heterochronic Genes on Variation in Developmental Time along an Altitudinal Cline of Drosophila melanogaster

Background

Previously, we have shown there is clinal variation for egg-to-adult developmental time along geographic gradients in Drosophila melanogaster. Further, we also have identified mutations in genes involved in metabolic and neurogenic pathways that affect development time (heterochronic genes). However, we do not know whether these loci affect variation in developmental time in natural populations.

Methodology/Principal Findings

Here, we constructed second chromosome substitution lines from natural populations of Drosophila melanogaster from an altitudinal cline, and measured egg-adult development time for each line. We found not only a large amount of genetic variation for developmental time, but also positive associations of the development time with thermal amplitude and altitude. We performed genetic complementation tests using substitution lines with the longest and shortest developmental times and heterochronic mutations. We identified segregating variation for neurogenic and metabolic genes that largely affected the duration of the larval stages but had no impact on the timing of metamorphosis.

Conclusions/Significance

Altitudinal clinal variation in developmental time for natural chromosome substitution lines provides a unique opportunity to dissect the response of heterochronic genes to environmental gradients. Ontogenetic stage-specific variation in invected, mastermind, cricklet and CG14591 may affect natural variation in development time and thermal evolution.     

Phenotypic plasticity in Drosophila cactophilic species: the effect of competition,density, and breeding sites

Changes in the environmental conditions experienced by naturally occurring populations are frequently accompanied by changes in adaptive traits allowing the organism to cope with environmental unpredictability. Phenotypic plasticity is a major aspect of adaptation and it has been involved in population dynamics of interacting species. In this study, phenotypic plasticity (i.e., environmental sensitivity) of morphological adaptive traits were analyzed in the cactophilic species Drosophila buzzatii and Drosophila koepferae (Diptera: Drosophilidae) considering the effect of crowding conditions (low and high density), type of competition (intraspecific and interspecific competition) and cacti hosts (Opuntia and Columnar cacti). All traits (wing length, wing width, thorax length, wing loading and wing aspect) showed significant variation for each environmental factor considered in both Drosophila species. The phenotypic plasticity pattern observed for each trait was different within and between these cactophilic Drosophila species depending on the environmental factor analyzed suggesting that body size‐related traits respond almost independently to environmental heterogeneity. The effects of ecological factors analyzed in this study are discussed in order to elucidate the causal factors investigated (type of competition, crowding conditions and alternative host) affecting the election of the breeding site and/or the range of distribution of these cactophilic species.     

Phenotypic plasticity for life history traits in Drosophila melanogaster. I. Effect on phenotypic and environmental correlations

All 36 possible crosses among 6 homozygous lines of Drosophila melanogaster were tested for their phenotypic response in developmental time and dry weight at eclosion to variation in temperature and yeast concentration. This method was chosen because it allows one to produce the same heterozygous offspring repeatedly for testing under more conditions than could be handled at once. We estimated the effects of yeast concentration and temperature and their interaction on both the phenotypic and the environmental components of variation and covariation of the two traits. Development was slower at low temperatures and yeast concentrations, and dry weight and viability were lower at higher temperatures and lower yeast levels. Interactions of the two factors with the crosses and with each other indicated that there were genetic differences in plasticity and that the sensitivity of a trait to one factor depended on the level of the other. The covariation of the two traits was generally weak within an environment. Across environments, its sign depended on the factor that changed between the environments: positive for temperature, negative for yeast concentration. These findings can be explained in terms of an established growth model for Drosophila larvae. We conclude that for plastic traits with moderate or low heritability, the relationship between the phenotypic and genetic covariance matrices may be a complex function of the environmental factors that affect the traits. Some implications for the prediction of the evolution in fluctuating environments are outlined.     

The quantitative genetic basis of clinal divergence in phenotypic plasticity

Phenotypic plasticity is thought to be an important mechanism for adapting to environmental heterogeneity. Nonetheless, the genetic basis of plasticity is still not well understood. In Drosophila melanogaster and D. simulans, body size and thermal stress resistance show clinal patterns along the east coast of Australia, and exhibit plastic responses to different developmental temperatures. The genetic basis of thermal plasticity, and whether the genetic effects underlying clinal variation in traits and their plasticity are similar, remains unknown. Here, we use line‐cross analyses between a tropical and temperate population of Drosophila melanogaster and D. simulans developed at three constant temperatures (18°C, 25°C, and 29°C) to investigate the quantitative genetic basis of clinal divergence in mean thermal response (elevation) and plasticity (slope and curvature) for thermal stress and body size traits. Generally, the genetic effects underlying divergence in mean response and plasticity differed, suggesting that different genetic models may be required to understand the evolution of trait means and plasticity. Furthermore, our results suggest that nonadditive genetic effects, in particular epistasis, may commonly underlie plastic responses, indicating that current models that ignore epistasis may be insufficient to understand and predict evolutionary responses to environmental change.