Jean-Philippe Morin

Phenotypic plasticity and developmental temperature in Drosophila: Analysis and significance of reaction norms of morphometrical traits

Abstract In ectotherm species like Drosophila, morphometrical quantitative traits exhibit a large amount of phenotypic plasticity as a consequence of developmental temperature. Generally the response curves called reaction norms, are non-linear and exhibit either single maxima or minima, or a sigmoid shape. Up to now, such complex shapes were mainly considered as non-adaptive, reflecting interactions between internal developmental constraints and the environment. We show that the general, all purpose method of polynomial adjustment provides a convenient way for the description of the norms. From the polynomial parameters, characteristic values with an obvious biological significance (e.g. the temperature of a maximum size), can be calculated and used for comparing populations or species. Experimental data on body pigmentation and body size show that the shapes of the reaction norms are genetically variable and suggest adaptive responses to the environment. The possible occurrence of specific regulatory genes acting on norm shape will be a matter for further investigations.

Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity

The two sibling cosmopolitan species, Drosophila melanogaster and D. simulans, are able to proliferate under very different climatic conditions. This has resulted in local adaptations, which are often arranged in latitudinal clines. Such clines are documented for body weight, wing and thorax length, sternopleural and abdominal bristle number, ovariole number and thoracic pigmentation. The overall magnitude of geographical differentiation is, however, much less in D. simulans than in D. melanogaster, and latitudinal clines are less pronounced.The fact that natural populations live under different climates raises the problem of interaction between temperature and phenotype. The reaction norms of morphometrical traits have been investigated as a function of growth temperature. The shapes of the response curves vary according to the investigated trait. They are generally curvilinear and can be described by calculating characteristic values after polynomial adjustments. For a given trait, the reaction norms of the two species are similar in their shape, although some significant differences may be observed.Within each species, significant differences are also observed between geographic populations: reaction norms are not parallel and the divergence is better marked when more distant populations (e.g., temperate and tropical) are compared. It thus appears that besides mean trait value, phenotypic plasticity is also a target of natural selection.A specific analysis of wing shape variation according to growth temperature was also undertaken. Reaction norms with different shapes may be observed in various parts of the wing: the major effect is found between the basis and the tip of the wing, but in a similar way in the two species. By contrast, some ratios, called wing indices by taxonomists, may exhibit completely different reaction norms in the two species.For a single developmental temperature (25°C) the phenotypic variability of morphometrical traits is generally similar in the two species, and also the genetic variability, estimated by the intraclass correlation. A difference exists, however, for the ovariole number which is less variable in D. simulans. Variance parameters may vary according to growth temperature, and a detailed analysis was made on wing dimensions. An increase of environmental variability at extreme, heat or cold temperatures, has been found in both species. Opposite trends were, however, observed for the genetic variability: a maximum heritability in D. simulans at middle temperatures, corresponding to a minimum heritability in D. melanogaster. Whether such a difference exists for other traits and in other populations deserves further investigations.In conclusion, morphometrical analyses reveal a large amount of significant differences which may be related to speciation and to the divergence of ecological niches. Within each species, numerous geographic variations are also observed which, in most cases, reflect some kinds of climatic adaptation.

Growth temperature and phenotypic plasticity in two Drosophila sibling species: probable adaptive changes in flight capacities

In the sibling species Drosophila melanogaster and D. simulans, growth and development at constant temperatures, from 12 to 30 °C, resulted in extensive variations of adult size and flight parameters with significant differences between species. Changes in body weight, thorax length and wing length were nonlinear, with maximum values of each trait at lower temperatures for D. simulans than for its sibling species. By contrast, the wing/thorax ratio and the wing loading varied monotonically with growth temperature. These traits were negatively correlated, the wing/thorax ratio decreasing with growth temperature while the wing loading increased. Wing/thorax ratio, which is easier to measure, thus appears as a convenient predictor of wing loading. During tethered flight at the same ambient temperature, the wingbeat frequency changed linearly as a function of the wing moment of inertia. More interestingly, the beat rate was strongly correlated with the increase of wing loading at growth temperature above 13 °C. The likely adaptive significance of these morphometrical changes for flight efficiency is discussed.

REACTION NORMS OF MORPHOLOGICAL TRAITS IN DROSOPHILA : ADAPTIVE SHAPE CHANGES IN A STENOTHERM CIRCUMTROPICAL SPECIES ?

Reaction norms of wing length, thorax length, and ovariole number were studied according to growth temperature in the circumtropical Drosophila ananassae, and compared to similar data from the cosmopolitan D. melanogaster. In the two species convex reaction norms were observed, but they were not parallel and sometimes exhibited intersections either at high (wing) or at low (thorax) temperature. On average, D. ananassae may be considered as a species with a bigger thorax but shorter wings than D. melanogaster. The shapes of reaction norms were analyzed and compared after quadratic polynomial adjustments. Significant differences were observed, in several cases between polynomial parameters, and in all cases between characteristic points that is, Maximum Value (MV) and Temperature of Maximum Value (TMV). The wing/thorax ratio may also be considered as a specific trait related to wing loading. Major differences were observed between the two species for the mean value and the shape of the response curves of this trait. The main observation of this work was however a shift of TMVs for wing and thorax length and ovariole number in D. ananassae toward higher temperatures. These variations in the reaction norms corresponded to a shift in the species thermal range, suggesting that temperature adaptation was accompanied by a modification of the shape of the response curves.

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 degrees C, to the warm-adapted D. melanogaster (mid thermal range at 22 degrees 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.

BODY SIZE AND DEVELOPMENTAL TEMPERATURE IN DROSOPHILA MELANOGASTER : ANALYSIS OF BODY WEIGHT REACTION NORM

Abstract 1. Phenotypic plasticity of body weight, wing and thorax length was analysed in ten isofemale lines of D. melanogaster grown at seven different temperatures (12–31°C). 2. For each trait, concave reaction norms were observed with a maximum at low temperature. The co-ordinates of the maximum were calculated after polynomial adjustments. 3. Body weight exhibited a specific reaction norm with a temperature of maximum value (16.7°C) intermediate between those of wing (14.9°C) and thorax (17.8°C). 5. Overall phenotypic plasticity according to temperature was high for weight and wing length but much less for thorax length. 5. In several aspects wing length might be a better predictor of body size variation than thorax length.

Body size reaction norms in Drosophila melanogaster: temporal stability and genetic architecture in a natural population

A natural population of Drosophila melanogaster was sampled twice over a 5-year interval from the same French locality in the same season. Reaction norms of wing and thorax length and wing/thorax ratio, according to growth temperature (12-31 °C) were analysed in ten isofemale lines for each sample. Reaction norms were very similar between years, showing not only a remarkable stability of the average size but also of the reactivity to temperature. Wing and thorax length reaction norms were characterized by the co-ordinates of their maxima (MV = maximum value of character; TMV = temperature of maximum value). The wing/thorax ratio, which exhibited a decreasing sigmoid norm, was characterized by the co-ordinates of the inflexion point. Again, these characteristic values were found to be very similar for samples between years. The results were further analysed by pooling the 20 lines into a single data set. Heritability was significantly variable according to temperature, but in a fairly irregular way with lowest values at extreme temperatures. Genetic variance of the three traits exhibited more regular variation with a minimum at intermediate temperatures and maxima at extreme high or low temperatures. Such was also the case of evolvability, i.e. the genetic coefficient of variation. Heritability and evolvability were found to be slightly but negatively correlated, showing that they provide independent biological information. The temporal stability of a natural population over the years suggests some stabilizing selection for both mean body size and plasticity. For laboratory evolution experiments, the natural origin population might be useful as a genetic control over time.

Phenotypic plasticity of body size in Drosophila: effects of a daily periodicity of growth temperature in two sibling species

Abstract. Variation of wing and thorax length under thermoperiodic growth conditions was analysed in four strains of two sibling species, Drosophila melanogaster and D. simulans, from two European localities. Results were compared to those obtained with constant temperatures ranging from 12 to 31 °C.

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.