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.     

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.     

GROWTH TEMPERATURE AND ADULT PIGMENTATION IN TWO DROSOPHILA SIBLING SPECIES: AN ADAPTIVE CONVERGENCE OF REACTION NORMS IN SYMPATRIC POPULATIONS?

Phenotypic plasticity of abdomen pigmentation was investigated in populations of the sibling species Drosophila melanogaster and D. simulans, living in sympatry in two French localities. Ten isofemale lines of each population and species were grown at different constant temperatures spanning their complete thermal range from 12 to 31°C. Genetic variability between isofemale lines was not affected by growth temperature, but was consistently less in D. simulans. For all traits, the dark pigmentation of the abdominal segments decreased according to growth temperature, in agreement with the thermal budget adaptive hypothesis. The shapes of the response curves were different between the abdominal segments, but for a given segment, quite similar in the two species. On average D. simulans was lighter than D. melanogaster, but the difference was mainly expressed at higher temperatures. An interesting result was the difference observed between the two localities: flies from the colder locality (Villeurbanne) were found to be darker than flies from the warmer locality (Bordeaux). Interestingly, this difference was expressed only at low temperatures, 21°C and below, that is, at temperatures encountered in natural conditions. This suggests an adaptive response resulting in a change of the shape of reaction norm and involving genotype-environment interactions. When comparing the genetic structure of geographic populations for quantitative traits, several laboratory environments should be preferred to a single one.     

EVOLUTION AND DEVELOPMENT OF BODY SIZE AND CELL SIZE IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE

We examined the evolutionary and developmental responses of body size to temperature in Drosophila melanogaster, using replicated lines of flies that had been allowed to evolve for 5 yr at 25°C or at 16.5°C. Development and evolution at the lower temperature both resulted in higher thorax length and wing area. The evolutionary effect of temperature on wing area was entirely a consequence of an increase in cell area. The developmental response was mainly attributable to an increase in cell area, with a small effect on cell number in males. Given its similarity to the evolutionary response, the increase in body size and cell size resulting from development at low temperature may be a case of adaptive phenotypic plasticity. The pattern of plasticity did not evolve in response to temperature for any of the traits. The selective advantage of the evolutionary and developmental responses to temperature is obscure and remains a major challenge for future work.     

Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila

As in most insect groups, host plant shifts in cactophilic Drosophila represent environmental challenges as flies must adjust their developmental programme to the presence of different chemical compounds and/or to a microflora that may differ in the diversity and abundance of yeasts and bacteria. In this context, wing morphology provides an excellent opportunity to investigate the factors that may induce changes during development. In this work, we investigated phenotypic plasticity and developmental instability of wing morphology in flies on the cactophilic Drosophila buzzatii and Drosophila koepferae raised on alternative breeding substrates. We detected significant differences in wing size between and within species, and between flies reared on different cactus hosts. However, differences in wing shape between flies emerged from different cactus hosts were not significant either in D. buzzatii or in D. koepferae. Our results also showed that morphological responses involved the entire organ, as variation in size and shape correlated between different portions of the wing. Finally, we studied the effect of the rearing cactus host on developmental instability as measured by the degree of fluctuating asymmetry (FA). Levels of FA in wing size were significantly greater in flies of both species reared in non-preferred when compared with those reared in preferred host cacti. Our results are discussed in the framework of an integrative view aimed at investigating the relevance of host plant shifts in the evolution of the guild of cactophilic Drosophila species that diversified in South America.     

The genetics of phenotypic plasticity. II. Response to selection

We selected on phenotypic plasticity of thorax size in response to temperature in Drosophila melanogaster using a family selection scheme. The results were compared to those of lines selected directly on thorax size. We found that the plasticity of a character does respond to selection and this response is partially independent of the response to selection on the mean of the character. One puzzling result was that a selection limit of zero plasticity was reached in the lines selected for decreased plasticity yet additive genetic variation for plasticity still existed in the lines. We tested the predictions of three models of the genetic basis of phenotypic plasticity: overdominance, pleiotropy, and epistasis. The results mostly support the epistasis model, that the plasticity of a character is determined by separate loci from those determining the mean of the character.     

Craniometrical variability and developmental stability. Two useful tools for assessing the population viability of Eurasian otter (Lutra lutra) populations in Europe.

Morphometrical univariate analyses of otter skulls collected over the past hundred years in European countries from presumed healthy populations were compared with skulls from presumed endangered populations. The average degree of sexual dimorphism of die European populations was found to be directly correlated to die skull size of die male otters. Fluctuating asymmetry (FA) in metric skull traits was analysed as an estimator of developmental stability. There was evidence for increased FA in different traits over time in some of the presumed endangered populations, and for a reduction in size of skull traits. In contrast, the healthy populations did not show any significant changes in the same traits during the same period. The reduced sexual dimorphism of the endangered populations is suggested to be a product of relaxed sexual selection and deteriorated habitat conditions. Environmental and genetic forces that may have shaped these patterns are discussed.     

Variations in body melanisation,ovariole number and fecundity in highland and lowland populations of Drosophila melanogaster from the Indian subcontinent

We investigated geographical variations in three fitness-related traits （body melanisation, ovariole number and fecundity） in laboratory-reared offspring of 10 populations of Drosophila melanogaster. The populations were collected from adjacent lowland and highland localities （-80-100 km apart） in the tropical as well as subtropical regions （11.15-31.06°N） covering a linear distance about 3 000 kilometers from south to north on the Indian subcontinent. Persistence of within- as well as between-population differences at 21 ℃ suggest that observed variations in fitness-related traits have a genetic basis. Populations from higher altitudes showed consistently higher trait values （1.4-fold increase） as compared with their corresponding lowland populations. By contrast, latitudinal variations were about two-fold higher across the entire continent. Along latitude as well as altitude, population means showed higher correlation values （r 〉 0.98） between all the three fitness traits. However, on the basis of within-population analysis （assorted darker and lighter flies）, changes in body melanisation were significantly correlated with fecundity but not with ovariole number. Thus, analysis of within-population trait variability should be preferred as compared with data on population means for adaptive significance of fitness-related traits. In the present study, the role of climatic selection is evident from regression analysis with changes in annual average temperature of the sites of origin of populations along latitude as well as altitude.     

Variations in body melanisation,ovariole number and fecundity in highland and lowland populations of Drosophila melanogaster from the Indian subcontinent

We investigated geographical variations in three fitness‐related traits (body melanisation, ovariole number and fecundity) in laboratory‐reared offspring of 10 populations of Drosophila melanogaster. The populations were collected from adjacent lowland and highland localities (～80–100 km apart) in the tropical as well as subtropical regions (11.15–31.06 °N) covering a linear distance about 3 000 kilometers from south to north on the Indian subcontinent. Persistence of within‐as well as between‐population differences at 21 °C suggest that observed variations in fitness‐related traits have a genetic basis. Populations from higher altitudes showed consistently higher trait values (1.4‐fold increase) as compared with their corresponding lowland populations. By contrast, latitudinal variations were about two‐fold higher across the entire continent. Along latitude as well as altitude, population means showed higher correlation values (r > 0.98) between all the three fitness traits. However, on the basis of within‐population analysis (assorted darker and lighter flies), changes in body melanisation were significantly correlated with fecundity but not with ovariole number. Thus, analysis of within‐population trait variability should be preferred as compared with data on population means for adaptive significance of fitness‐related traits. In the present study, the role of climatic selection is evident from regression analysis with changes in annual average temperature of the sites of origin of populations along latitude as well as altitude.     

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.     

ADAPTATION TO FERMENTING RESOURCES IN DROSOPHILA MELANOGASTER: ETHANOL AND ACETIC ACID TOLERANCES SHARE A COMMON GENETIC BASIS

Ethanol and acetic acid tolerances were compared in a French, highly tolerant population, and in a Congolese, very sensitive population. For both tolerances, chromosome substitutions demonstrated a major effect on chromosome 3, a lesser effect on chromosome 2, and no effect on chromosome 1, except in interactions. Directional selection experiments led to significant increases of tolerance to both toxics. Of greater interest, a strong correlated response was observed in each line: increased ethanol tolerance was accompanied by higher acetic acid tolerance and vice versa. A high genetic correlation (average value r = 0.77) was found between the two traits. These data suggest that alcohol dehydrogenase (ADH) activity does not play a major role in explaining the physiological differences known between Afrotropical and European populations. The metabolic flux permitting the detoxification of ethanol and acetic acid seems to be mainly controlled by acetyl-coA synthetase (ACS) at least in adult flies. Acetic acid adaptation could be as important as ethanol adaptation in the ecology of Drosophila melanogaster and other Drosophila species.     

Sexual differences in growth strategies of the wolf spider Hygrolycosa rubrofasciata

In invertebrates, the size at maturation is considered to be important for adult fitness. In the wolf spider Hygrolycosa rubrofasciata, however, it is only females that clearly benefit of larger size through augmented egg production, while male mating success is determined by display activity not related to size. Thus, we can expect conflicting growth patterns for the sexes. Additionally, populations differ greatly in adult size: individuals from dry habitats are smaller than those from wet habitats. To study the sexual differences in reaction norms of growth, we reared spiderlings from seven populations at two food levels under controlled laboratory conditions and compared size at sexual maturity. The shapes of reaction norms for adult size differed between the sexes. In females, the reaction norms were parallel, but individuals from dry habitats tended to grow larger at the given food levels. In males, there was a significant interaction between food level and population without any consistent differences between populations. Maturation time was a plastic character in both sexes with no genetic differences among populations. However, females on low food level matured later and significantly smaller in size than those on high food level. Males also matured later on low food level, but they were nearly of the same size as males that received more food. Female growth patterns reflected the strong selection for large size at maturity. However, the patterns for males were highly variable, which could be explained by the weak overall selection on male size, which means that any environmental factors can affect male growing patterns. This revised version was published online in November 2006 with corrections to the Cover Date.