Developmental constraints and wing shape variation in natural populations of Drosophila melanogaster (original) (raw)

TEMPERATURE-RELATED DIVERGENCE IN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER. I. GENETIC AND DEVELOPMENTAL BASIS OF WING SIZE AND SHAPE VARIATION

The effects of environmental temperature on wing size and shape of Drosophila melanogaster were analyzed in populations derived from an Oregon laboratory strain kept at three temperatures (IS0, 25", 28") for 4 yr. Temperature-directed selection was identified for both wing size and shape. The length of the four longitudinal veins, used as a test for wing size variations in the different populations, appears to be affected by both genetic and maternal influences. Vein expression appears to be dependent upon developmental pattern of the wing: veins belonging to the same compartment are coordinated in their expression and relative position, whereas veins belonging to different compartments are not. Both wing and cell areas show genetic divergence, particularly in the posterior compartment. Cell number seems to compensate for cell size variations. Such compensation is carried out both at the level of single organisms and at the level of population as a whole. The two compartments behave as individual units of selection.

Temperature-related divergence in experimental populations of Drosophila melanogaster. II. Correlation between fitness and body dimensions

Journal of Evolutionary Biology, 1989

The effects of environmental temperature on wing size and shape of Drosophila melanogaster were analyzed in populations derived from an Oregon laboratory strain kept at three temperatures (IS0, 25", 28") for 4 yr. Temperature-directed selection was identified for both wing size and shape. The length of the four longitudinal veins, used as a test for wing size variations in the different populations, appears to be affected by both genetic and maternal influences. Vein expression appears to be dependent upon developmental pattern of the wing: veins belonging to the same compartment are coordinated in their expression and relative position, whereas veins belonging to different compartments are not. Both wing and cell areas show genetic divergence, particularly in the posterior compartment. Cell number seems to compensate for cell size variations. Such compensation is carried out both at the level of single organisms and at the level of population as a whole. The two compartments behave as individual units of selection.

Temperature-related divergence in experimental populations of Drosophila melanogaster. III. Fourier and centroid analysis of wing shape and relationship between shape variation and fitness

Journal of Evolutionary Biology, 1991

From a laboratory stock of Drosophila melanogaster (Oregon), reared for more than 20 years at lX"C, two new populations were derived and maintained at 25" and 28°C for 8 years. The chromosomal and cytoplasmic contribution to genetic divergence between the two more extreme populations was estimated at 18°C and 28°C. Wing shape and two fitness components (fecundity and fertility) were taken into account. Fourier descriptors and the position of the centroid were taken as indicators either of wing shape variation, determined by a different response of the two wing compartments to temperature selection, or of wing shape variation determined by both compartments. The descriptors appear to be good characters: they show a variability which is genetically controlled and ascribable to genes located on specific chromosomes. The third chromosome is responsible for the adaptive difference to temperature. The genes which control wing shape are located on the second and third chromosome, although the contribution of each chromosome depends on the environment in which the flies develop. Cytoplasmic genes display an effect as large as that of chromosomes, and nucleus x cytoplasm interaction is present. The correlation between the genetic contributions to compartment-dependent wing shape variation and the contributions to fitness is highly significant, especially at 28°C. Wing shape has, therefore, an adaptive significance in relation to temperature, which is particularly expressed in the environment where selection occurred.

Cellular basis of morphological variation and temperature-related plasticity in Drosophila melanogaster strains with divergent wing shapes

Genetica, 2014

Organ shape evolves through cross-generational changes in developmental patterns at cellular and/or tissue levels that ultimately alter tissue dimensions and final adult proportions. Here, we investigated the cellular basis of an artificially selected divergence in the outline shape of Drosophila melanogaster wings, by comparing flies with elongated or rounded wing shapes but with remarkably similar wing sizes. We also tested whether cellular plasticity in response to developmental temperature was altered by such selection. Results show that variation in cellular traits is associated with wing shape differences, and that cell number may play an important role in wing shape response to selection. Regarding the effects of developmental temperature, a size-related plastic response was observed, in that flies reared at 16°C developed larger wings with larger and more numerous cells across all intervein regions relative to flies reared at 25°C. Nevertheless, no conclusive indication of altered phenotypic plasticity was found between selection strains for any wing or cellular trait. We also described how cell area is distributed across different intervein regions. It follows that cell area tends to decrease along the anterior wing compartment and increase along the posterior one. Remarkably, such pattern was observed not only in the selected strains but also in the natural baseline population, suggesting that it might be canalized during development and was not altered by the intense program of artificial selection for divergent wing shapes.

Genetic architecture of wing morphology in Drosophila simulans and an analysis of temperature effects on genetic parameter estimates

Heredity, 2004

The Drosophila wing has been used as a model to investigate the mechanisms responsible for size and shape changes in nature, since such changes might underlie morphological evolution. To improve the understanding of wing morphological variation and the interpretation of genetic parameters estimates, we have established 59 lines from a Drosophila simulans laboratory population through single pair random matings. The offspring of each line were reared at three different temperatures, and the wing morphology of 12 individuals was analyzed by adjusting an ellipse to the wings' contour. Temperature, sex and line significantly affected wing trait variation, which was mainly characterized by longer wings having the second, fourth and fifth longitudinal veins closer together at the wing tip. As for the genetic parameter estimates, while the cross-environment heritability of some traits, such as wing size (SI), decreased with an increasing difference between the temperatures at which parents and offspring were reared, wing shape (SH) heritability did not seem to change. Since we found indications that neither an increase in the phenotypic variation nor the occurrence of genotype-environment interactions could fully explain the low heritabilities of SI estimated by cross-environment regressions, we discuss the importance of other effects for explaining this discrepancy between the SI and SH heritability estimates. In addition, although the genetic matrix was not entirely represented in the phenotypic matrix, several correspondences were identified, suggesting that the observed patterns of wing morphology variation are genetically controlled.

ALLOMETRIC AND NONALLOMETRIC COMPONENTS OF DROSOPHILAWING SHAPE RESPOND DIFFERENTLY TO DEVELOPMENTAL TEMPERATURE

Phenotypic plasticity of wing size and shape of Drosophila simulans was analyzed across the entire range of viable developmental temperatures with Procrustes geometric morphometric method. In agreement with previous studies, size clearly decreases when temperature increases. Wing shape variation was decomposed into its allometric (24%) and nonallometric (76%) components, and both were shown to involve landmarks located throughout the entire wing blade. The allometric component basically revealed a progressive, monotonous variation along the temperature. Surprisingly, nonallometric shape changes were highly similar at both extremes of the thermal range, suggesting that stress, rather than temperature per se, is the key developmental factor affecting wing shape.

Antagonistic selection between adult thorax and wing size in field released Drosophila melanogaster independent of thermal conditions

Journal of Evolutionary Biology, 2007

Attempts to explain size variation in Drosophila and other small insects often focus on the larval stage and association between development time and size, but patterns are also influenced by direct selection on size-related traits in the adults. Here we use multiple field releases of Drosophila melanogaster to test the association between size and one component of field fitness, the ability of Drosophila to locate resources for feeding and breeding. We find antagonistic selection between wing length and thorax length in both males and females, such that capture at baits is higher for flies with relatively larger thorax lengths and smaller wings. However flies with large wings relative to thoraces disperse further as reflected in the longer distances moved to baits. These patterns did not depend strongly on weather conditions, suggesting that selection on adult size is at least partly independent of temperature. Antagonistic selection between size traits can generate changes in size along gradients if the distribution of resources in the environment varies and selects for different dispersal patterns, particularly as dispersal is relatively higher under warmer conditions.

Opposite environmental and genetic influences on body size in North American Drosophila pseudoobscura

BMC Evolutionary Biology, 2015

Background: Populations of a species often differ in key traits. However, it is rarely known whether these differences are associated with genetic variation and evolved differences between populations, or are instead simply a plastic response to environmental differences experienced by the populations. Here we examine the interplay of plasticity and direct genetic control by investigating temperature-size relationships in populations of Drosophila pseudoobscura from North America. We used 27 isolines from three populations and exposed them to four temperature regimes (16°C, 20°C, 23°C, 26°C) to examine environmental, genetic and genotype-by-environment sources of variance in wing size. Results: By far the largest contribution to variation in wing size came from rearing temperature, with the largest flies emerging from the coolest temperatures. However, we also found a genetic signature that was counter to this pattern as flies originating from the northern, cooler population were consistently smaller than conspecifics from more southern, warmer populations when reared under the same laboratory conditions. Conclusions: We conclude that local selection on body size appears to be acting counter to the environmental effect of temperature. We find no evidence that local adaptation in phenotypic plasticity can explain this result, and suggest indirect selection on traits closely linked with body size, or patterns of chromosome inversion may instead be driving this relationship.

Seasonal variation in wing size and shape of Drosophila melanogaster reveals rapid adaptation to environmental changes

Scientific Reports

Populations in seasonal fluctuating environments receive multiple environmental cues and must deal with this heterogenic environment to survive and reproduce. An enlarged literature shows that this situation can be resolved through rapid adaptation in Drosophila melanogaster populations. Long-term monitoring of a population in its natural habitat and quantitative measurement of its responses to seasonal environmental changes are important for understanding the adaptive response of D. melanogaster to temporal variable selection. Here, we use inbred lines of a D. melanogaster population collected at monthly intervals between May to October over a temporal scale spanning three consecutive years to understand the variation in wing size and wing shape over these timepoints. The wing size and shape of this population changed significantly between months and a seasonal cycle of this traits is repeated for three years. Our results suggest that the effects of environmental variables that gen...