Phenotypic plasticity of body pigmentation in Drosophila melanogaster: genetic repeatability of quantitative parameters in two successive generations

In Drosophila melanogaster, body pigmentation is a quantitative trait that depends on developmental temperature. When investigated over the whole thermal range of the species, pigmentation exhibits nonlinear reaction norms that differ among segments. The isofemale line method was used to analyse the genetic variability in two natural populations that affected the shape of reaction norms. Each line was considered as an experimental repeat, and polynomial reaction norms fitted to calculate the characteristic values (eg the coordinates of a maximum). In total, 20 lines from two geographically distant populations (France and India) were investigated at seven developmental temperatures (12-31 degrees C) in two successive generations (G2 and G3). We analysed the genetic repeatability (ie the correlation between generations) of three kinds of parameters: intraclass correlation coefficients (isofemale heritability), family means at different temperatures and the characteristic values of the reaction norms. For intraclass correlation, a low genetic repeatability was found. For family mean values grown at various temperatures, an overall positive and highly significant repeatability was found (r=0.55+/-0.024). Finally, a positive significant G2-G3 correlation was also the rule for the characteristic values of the reaction norms. Significant differences could be found between values describing either the trait or its plasticity, but with no general trend. A slightly higher repeatability was observed in the Indian population. These results show that, with a family selection design, the shape of the reaction norms might be modified in various ways.     

The genetics of phenotypic plasticity. IX. Genetic architecture, temperature, and sex differences in Drosophila melanogaster

Abstract.— We examined the genetic architecture of plasticity of thorax and wing length in response to temperature in Drosophila melanogaster . Reaction norms as a function of growth temperature were analyzed in 20 isofemale lines in a natural population collected from Grande Ferrade near Bordeaux (southern France) in two different years. We found evidence for a complex genetic architecture underlying the reaction norms and differences between males and females. Reaction norms were negative quadratics. Genetic correlations were moderately high between traits within environments. Among characteristic values, the magnitudes of genetic correlations varied among traits and sexes. We hypothesized that genetic correlations among environments would decrease as temperatures became more different. This expectation was upheld for only one trait, female thorax length. For males for both traits, the correlations were large for both very similar and very different temperatures. These correlations may constrain the evolution of the shape of the reaction norms. Whether the extent of independence implies specific regulatory genes or only a specific allelic regulation of trait genes can not be decided from our results.     

Phenotypic plasticity of sternopleural bristle number in temperate and tropical populations of Drosophila melanogaster

We investigated the phenotypic plasticity of sternopleural bristle (SB) number as a function of growth temperature in isofemale lines from temperate (France) and tropical (Congo) populations of Drosophila melanogaster. We found concave reaction norms with a maximum in the middle of the thermal range, except in four African lines which exhibited a regularly decreasing response curve. Genetic variability (intraclass correlation) and evolvability (genetic CV, coefficient of variation) were independent properties and did not change with temperature. Residual, within-line variability was, however, strongly influenced by growth temperature, showing a U-shaped response curve and a minimum CV of 9% at 21.5 degrees C. As expected from a previously known latitudinal cline, maximum values (MV) were higher in temperate than in tropical flies. The temperature of maximum value (TMV) was observed at a higher temperature in the tropical population, in agreement with similar adaptive trends already observed for other quantitative traits. Significant negative correlations within each population were observed between a plasticity curvature parameter and MV or TMV. No difference in curvature was, however, observed between populations, in spite of their very different MVs.     

Genetic Variation in Foraging Traits and Life-History Traits of the Predatory Mite Neoseiulus womersleyi (Acari: Phytoseiidae) among Isofemale Lines

The predatory mite Neoseiulus womersleyi shows a significant correlation between its olfactory response and dispersal tendency in different geographical populations. This study investigated the genetic background of the relationship using isofemale lines. Y-tube olfactometer tests confirmed that there was a genetic component in predator response to herbivore-induced plant volatiles. Wind tunnel tests in the absence of the herbivore-induced plant volatiles revealed that the dispersal tendencies of N. womersleyi exhibited genetic variation among isofemale lines, and other experiments revealed the existence of significant differences in prey consumption rate, fecundity, and developmental time. However, there was no genetic correlation between behavioral traits (olfactory response, innate dispersal) and the other traits, suggesting that the positive correlation between the behavioral traits was not caused by genetic factors.     

Quantitative trait analysis and geographic variability of natural populations of Zaprionus indianus, a recent invader in Brazil

Five natural samples of a recent South America invader, the drosophilid Zaprionus indianus, were investigated with the isofemale line technique. These samples were compared to five African mainland populations, investigated with the same method. The results were also compared to data obtained on mass cultures of other populations from Africa and India. Three quantitative traits were measured on both sexes, wing and thorax length and sternopleural bristle number. We did not find any latitudinal trend among the American samples, while a significant increase in body size with latitude was observed in the Indian and, to a lesser degree, in the African populations. American populations were also characterized by their bigger size. Genetic variability, estimated by the intraclass correlation among isofemale lines, was similar in American and African populations. The intraline, nongenetic variability was significantly less in the American samples, suggesting a better developmental stability, the origin of which is unclear. A positive relationship was evident between intraline variability of size traits and the wing-thorax length correlation. Altogether, our data suggest that the colonizing propagule introduced to Brazil had a fairly large size, preventing any bottleneck effect being detected. The big body size of American flies suggests that they came from a high-latitude African country. The lack of a latitudinal dine in America seems to be related to the short time elapsed since introduction. The very rapid spread of Z. indianus all over South America suggests that it might rapidly invade North America.     

Quantitative morphometrical analysis of a North African population of <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>: sexual dimorphism,and comparison with European populations

Genetic variability of quantitative traits was investigated in aMoroccan population of Drosophila melanogaster, with an isofemale line design. Results were compared with data previously obtained from French populations. Although the environmental and thermal conditions are very different in France and Morocco, only two significant differences were observed: a shorter wing and a lighter abdomen pigmentation in Morocco. It is, therefore, concluded that Moroccan D. melanogaster are quite typical temperate flies, belonging to the Palaearctic region, and very different from the ancestral Afrotropical populations. Almost all traits were genetically variable, as shown by significant intraclass correlations among lines. Genetic correlations were highly significant among three size-related traits, while much lower between size and bristle numbers. Fluctuating asymmetry was greater for abdominal bristles than for sternopleural bristles. Sex dimorphism, analysed as a female/male ratio, was identical in French and Moroccan populations. Examination of the thorax length/thorax width ratio showed that the thorax is more elongated in females. Sexual dimorphism of wing length was significantly more correlated to thorax width than to thorax length. The results illustrate the value of measuring numerous quantitative traits on the same flies for characterizing the genetic architecture of a natural population. In several cases, and especially for genetic correlations, some interesting suggestions could be made, which should be confirmed, or invalidated, by more extensive investigations.     

Growth temperature and genetic variability of wing dimensions in Drosophila: opposite trends in two sibling species

Thirteen linear wing dimensions were measured in 10 isofemale lines of Drosophila melanogaster and D. simulans grown at seven constant temperatures from 12 to 31 degrees C. Within-line (environmental) variability, estimated by the within-line coefficient of variation (CVw), exhibited similar variation patterns in the two species, that is higher values at extreme (low or high) temperatures. The magnitude of variation was, however, greater in D. simulans, which appears to be more responsive to thermal change. A clear hyperbolic relationship between trait mean value and CVw was also observed in both species, arising from measurement errors which are relatively more pronounced on shorter traits. Genetic variability was analysed by considering both the genetic CV (CVg, evolvability) and isofemale line heritability (intraclass correlation). Both parameters provided independent information, as shown by a lack of correlation between them. Moreover, CVg was negatively correlated with trait mean value, while heritability showed a positive correlation. With respect to thermal environment, both parameters exhibited similar reaction patterns which contrasted the two species. Genetic variability in D. melanogaster followed a convex reaction norm, with higher values at extreme (high or low) temperatures, and this observation agrees with previous independent investigations. Surprisingly, D. simulans revealed an opposite pattern, with a maximum genetic variability in the middle of the range. Such data point to the danger of drawing general conclusions from the analysis of a single species.     

Fluctuating asymmetry of meristic traits: an isofemale line analysis in an invasive drosophilid, <Emphasis Type="Italic">Zaprionus indianus</Emphasis>

Metric (e.g., body size) and meristic (e.g., bristle number) traits are of general use in quantitative genetic studies, and the phenotypic variance is subdivided into a genetic and a non-genetic environmental component. The non-genetic variance may have two origins: a common garden effect between individuals and a developmental instability within the same individual. Developmental instability may be studied by considering the fluctuating asymmetry (FA) between the two sides of the body. The isofemale line technique is a convenient method for investigating the architecture of natural populations but has been rarely implemented for investigating FA. In this paper, we use this experimental design for analyzing four meristic traits in eight populations of the cosmopolitan Zaprionus indianus. A study of the correlation between left and right side of each line revealed that almost 90% of the variability was due to a developmental noise, while a much higher correlation among the means of the lines from the same population was observed. A slight trend toward a directional asymmetry was observed: more thoracic bristles on the left side. Four kinds of indices, scaled or non-scaled to the mean were used for comparing the different traits. Unscaled values (mean absolute values or standard deviation of each line) revealed a linear increase with the means. Interestingly the results of ovariole number were included in the same regression. With the scaled indices (mean absolute divided by each individual value or stadard deviation devided by the mean), the differences among traits were considerably decreased, but still remained significant. The mean FA of the various traits were not correlated, suggesting that each trait harbors its own developmental stability. The CVs of FA were high with a magnitude similar to those of the trait themselves, slightly less than 10%. Finally, even with the isofemale line design, which is a powerful means for unravelling slight genetic variations, we did not to find any clear indication of a genetic component of FA under the optimal environmental conditions used in this study.     

Quantitative variation of four morphological traits in Drosophila melanogaster under larval crowding

Effects of three different larval densities (low, intermediate and high) on phenotypic and genetic variation of four morphological traits (thorax and wing length, sternopleural and abdominal bristle number) were studied in Drosophila melanogaster using the isofemale line technique. Phenotypic variation was found to increase at high larval density in all traits examined. Environmental variance for three traits (exception was sternopleural bristle number) and fluctuating asymmetry for both bilateral traits were also increased under high density conditions. For estimates of genetic variability (among isofemale lines variance, heritability and evolvability), no statistically significant differences among density regimes were detected. However, the trends in changes of these estimates across densities indicated a possibility for enhanced genetic variation under larval crowding for all traits except abdominal bristle number. For the latter trait, genetic variation seemed not to be dependent on density regime. Generally, two metric traits (thorax and wing length) were more affected by larval crowding than two meristic ones (sternopleural and abdominal bristle number). The Results are in complete agreement with those previously obtained for D. melanogaster using extreme temperatures as stress-factors.     

Genetic correlation between temperature-induced plasticity of life-history traits in a soil arthropod

Temperature is considered one of the most important mediators of phenotypic plasticity in ectotherms. However, the costs and benefits shaping the evolution of different thermal responses are poorly elucidated. One of the possible constraints to phenotypic plasticity is its intrinsic genetic cost, such as genetic linkage or pleiotropy. Genetic coupling of the thermal response curves for different life history traits may significantly affect the evolution of thermal sensitivity in thermally fluctuating environments. We used the collembolan Orchesella cincta to study if there is genetic variation in temperature-induced phenotypic plasticity in life history traits, and if the degree of temperature-induced plasticity is correlated across traits. Egg development rate, juvenile growth rate and egg size of 19 inbred isofemale lines were measured at two temperatures. Our results show that temperature was a highly significant factor for all three traits. Egg development rate and juvenile growth rate increased with increasing temperature, while egg size decreased. Line by temperature interaction was significant for all traits tested; indicating that genetic variation for temperature-induced plasticity existed. The degree of plasticity was significantly positively correlated between egg development rate and growth rate, but plasticity in egg size was not correlated to the other two plasticity traits. The findings suggest that the thermal plasticities of egg development rate and growth rate are partly under the control of the same genes or genetic regions. Hence, evolution of the thermal plasticity of traits cannot be understood in isolation of the response of other traits. If traits have similar and additive effects on fitness, genetic coupling between these traits may well facilitate the evolution of optimal phenotypes. However, for this we need to know the selective forces under field conditions.     

PHENOTYPIC PLASTICITY AND REACTION NORMS IN TEMPERATE AND TROPICAL POPULATIONS OF DROSOPHILA MELANOGASTER: OVARIAN SIZE AND DEVELOPMENTAL TEMPERATURE

The plasticity of ovariole number relative to developmental temperature was studied in three populations of Drosophila melanogaster at both ends of the cline: a temperate French population and two equatorial Congolese. Ovary size was much greater in the French flies, in agreement with an already known latitudinal cline. Among isofemale lines, significant differences in genetic variability were observed between populations with a maximum variability at intermediate temperatures. Parameters of phenotypic variability (CV and FA) were not statistically different among lines or populations, but a significant increase at low temperature was demonstrated for both. The shapes of the response curves (i.e., the norm of reaction) were analyzed by adjusting the data to a quadratic equation. The parameters of the equation were highly variable among lines. On the other hand, the temperature for maximum value of ovarioles (TMV) was much less variable and exhibited only a slightly significant difference between temperate and tropical flies (22.2°C vs. 22.7°C). During its geographic extension toward colder places, D. melanogaster underwent a large, presumably adaptative, increase in ovariole number but very little change in the norm of reaction of that trait.     

Genotype by environment interactions in viability and developmental time in populations of cactophilic Drosophila

The genetic and ecological basis of viability and developmental time differences between Drosophila buzzatii and D. koepferae were analysed using the isofemale line technique. Several isofemale lines were sampled from pairs of allopatric/sympatric populations of each species. Flies were reared in media prepared with decaying tissues of two of the main natural cactus hosts of each species. This experimental design enabled us to evaluate the relative contribution of phenotypic plasticity, genetic variation and genotype by environment interaction (G x E) to total phenotypic variation for two fitness traits, viability and developmental time. Our results revealed significant G x E in both traits, suggesting that the maintenance of genetic variation can be explained, at least in part, by diversifying selection in different patches of a heterogeneous environment in both species. However, the relative importance of the factors involved in the G x E varied between traits and populations within species. For viability, the G x E can be mainly attributed to changes in the rank order of lines across cacti. However, the pattern was different for developmental time. In D. buzzatii the G x E can be mainly accounted for by changes in among line variance across cacti, whereas changes in the rank order of lines across cacti was the main component in D. koepferae. These dissimilar patterns of variation between traits and species suggest that the evolutionary forces shaping genetic variation for developmental time and viability vary between populations within species and between species.     

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.     

Latitudinal Variation in Starvation Resistance is Explained by Lipid Content in Natural Populations of Drosophila melanogaster

One of the most common environmental stressors is a shortage or suboptimal quality of food, thus all animals deal with periods of starvation. In the present study we examine variation in starvation resistance, longevity and body lipid content and the correlations between traits along an environmental gradient using isofemale lines recently derived from natural populations of Drosophila melanogaster from South America. The use of isofemale lines and controlled rearing laboratory conditions allows us to investigate within and among population components of genetic variation and the potential associations among starvation resistance, longevity and body lipid content. All these traits were analyzed separately in females and males, improving our understanding of sexual dimorphism. Our results revealed significant differences among populations in starvation resistance and longevity. Actually, the opposing latitudinal cline detected for starvation resistance suggests that natural selection played an essential role in shaping the pattern of geographic variation in this trait. Moreover, we also detected a positive relationship between starvation resistance and body lipid content in both sexes, providing evidence for a physiological and/or evolutionary association between these traits. Conversely, starvation resistance was not correlated with longevity indicating that these traits might be enabled to evolve independently. Finally, our study reveals that there is abundant within population genetic variation for all traits that may be maintained by sex-specific effects.     

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.     

Phenotypic plasticity and reaction norms of abdominal bristle number inDrosophila melanogaster

The phenotypic plasticity of abdominal bristle number (segments 3 and 4 in females) was investigated in 10 isofemale lines from a French population, grown at 7 constant temperatures, ranging from 12‡ to 31‡C. Overall concave reaction norms were obtained with a maximum around 20‡-21‡C. Intraclass correlation (isofemale line heritability) was not affected by temperature. Correlations between segments 3 and 4 strongly contrasted a low within-line phenotypic correlation (r = 0.39 ± 0.04) and a high, between-line genetic correlation (r = 0.89 ± 0.03). A significant decrease of the genetic correlation was observed when comparing more different temperatures. Finally, among 7 other morphometrical traits which were measured on the same set of lines, 3 provided a significant positive genetic correlation with abdominal bristles: thoracic bristles, abdomen pigmentation and thoracic pigmentation.     

Within-population variation in body size plasticity in response to combined nutritional and thermal stress is partially independent from variation in development time

Ongoing climate change has forced animals to face changing thermal and nutritional environments. Animals can adjust to such combinations of stressors via plasticity. Body size is a key trait influencing organismal fitness, and plasticity in this trait in response to nutritional and thermal conditions varies among genetically diverse, locally adapted populations. The standing genetic variation within a population can also influence the extent of body size plasticity. We generated near-isogenic lines from a newly collected population of Drosophila melanogaster at the mid-point of east coast Australia and assayed body size for all lines in combinations of thermal and nutritional stress. We found that isogenic lines showed distinct underlying patterns of body size plasticity in response to temperature and nutrition that were often different from the overall population response. We then tested whether plasticity in development time could explain, and therefore regulate, variation in body size to these combinations of environmental conditions. We selected five genotypes that showed the greatest variation in response to combined thermal and nutritional stress and assessed the correlation between response of developmental time and body size. While we found significant genetic variation in development time plasticity, it was a poor predictor of body size among genotypes. Our results therefore suggest that multiple developmental pathways could generate genetic variation in body size plasticity. Our study emphasizes the need to better understand genetic variation in plasticity within a population, which will help determine the potential for populations to adapt to ongoing environmental change.     

Ontogenetic plasticity of anatomical and ecophysiological traits and their correlations in Iris pumila plants grown in contrasting light conditions

To better understand what directs and limits the evolution of phenotype, constraints in the realization of the optimal phenotype need to be addressed. That includes estimations of variability of adaptively important traits as well as their correlation structures, but also evaluation of how they are affected by relevant environmental conditions and development phases. The aims of this study were to analyze phenotypic plasticity, genetic variability and correlation structures of important Iris pumila leaf traits in different light environments and ontogenetic phases, and estimate its evolutionary potential. Stomatal density, specific leaf area, total chlorophyll concentration and chlorophyll a/b ratio were analyzed on I. pumila full‐sib families in the seedling phase and on the same plants after 3 years of growth in contrasting light conditions typical for ontogenetic stage in question. There was a significant phenotypic plasticity in both ontogenetic stages, but significant genetic variability was detected only for chlorophyll concentrations. Correlations of the same trait between different stages were weak due to changes in environmental conditions and difference in ontogenetic reaction norms of different genotypes. Ontogenetic variability of correlation structures was detected, where correlations and integration were higher in seedlings compared with adult plants 3 years later. Correlations were affected by environmental conditions, with integration being higher in the lower light conditions, but correlations between phases being stronger in the higher light treatment. These findings demonstrated that the analyzed traits can be selected and can mostly evolve independently in different environments and ontogenetic stages, with low genetic variability as a potentially main constraint.     

Plasticity Regulators Modulate Specific Root Traits in Discrete Nitrogen Environments

Plant development is remarkably plastic but how precisely can the plant customize its form to specific environments? When the plant adjusts its development to different environments, related traits can change in a coordinated fashion, such that two traits co-vary across many genotypes. Alternatively, traits can vary independently, such that a change in one trait has little predictive value for the change in a second trait. To characterize such “tunability” in developmental plasticity, we carried out a detailed phenotypic characterization of complex root traits among 96 accessions of the model Arabidopsis thaliana in two nitrogen environments. The results revealed a surprising level of independence in the control of traits to environment – a highly tunable form of plasticity. We mapped genetic architecture of plasticity using genome-wide association studies and further used gene expression analysis to narrow down gene candidates in mapped regions. Mutants in genes implicated by association and expression analysis showed precise defects in the predicted traits in the predicted environment, corroborating the independent control of plasticity traits. The overall results suggest that there is a pool of genetic variability in plants that controls traits in specific environments, with opportunity to tune crop plants to a given environment.     

Constraints on the evolution of adaptive plasticity: costs of plasticity to density are expressed in segregating progenies

Phenotypic plasticity, the ability of a genotype to express different phenotypes across environments, is an adaptive strategy expected to evolve in heterogeneous environments. One widely held hypothesis is that the evolutionary benefits of plasticity are reduced by its costs, but when compared with the number of traits tested, the evidence for costs is limited. Selection gradients were calculated for traits and trait plasticities to test for costs of plasticity to density in a field study using recombinant inbred lines (RILs) of Brassica rapa. Significant costs of putatively adaptive plasticity were found in three out of six measured traits. For one trait, petiole length, a cost of plasticity was detected in both environments tested; such global costs are expected to more strongly constrain the evolution of plasticity than local costs expressed in a single environment. These results, in combination with evidence from studies in segregating progenies of Arabidopsis thaliana, suggest that the potential for genetic costs of plasticity exists in natural populations. Detection of costs in previous studies may have been limited because historical selection has purged genotypes with costly plasticity, and experimental conditions often lack environmental stresses.