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

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.     

An interspecific QTL study of Drosophila wing size and shape variation to investigate the genetic basis of morphological differences

The Drosophila wing has been used as a model in studies of morphogenesis and evolution; the use of such models can contribute to our understanding of mechanisms that promote morphological divergence among populations and species. We mapped quantitative trait loci (QTL) affecting wing size and shape traits using highly inbred introgression lines between D. simulans and D. sechellia, two sibling species of the melanogaster subgroup. Eighteen QTL peaks that are associated with 12 wing traits were identified, including two principal components. The wings of D. simulans and D. sechellia significantly diverged in size; two of the QTL peaks could account for part of this interspecific divergence. Both of these putative QTLs were mapped at the same cytological regions as other QTLs for intraspecific wing size variation identified in D. melanogaster studies. In these regions, one or more loci could account for intra- and interspecific variation in the size of Drosophila wings. Three other QTL peaks were related to a pattern of interspecific variation in wing size and shape traits that is summarized by one principal component. In addition, we observed that female wings are significantly larger and longer than male wings and the second, fourth and fifth longitudinal veins are closer together at the distal wing area. This pattern was summarized by another principal component, for which one QTL was mapped.     

Wing shape heritability and morphological divergence of the sibling species Drosophila mercatorum and Drosophila paranaensis

The fruit-flies Drosophila paranaensis and Drosophila mercatorum pararepleta are sibling species belonging to the repleta group. Females of these two species are normally considered to be morphologically indistinguishable while males only differ consistently in the morphology of their genitalia. These species are sympatric throughout a large area of their geographic distribution. In this study, we investigated the degree of morphological divergence between D. paranaensis and D. mercatorum pararepleta based on morphometric analysis of their wings. The ellipse method was used to describe the placement of the longitudinal and transversal wing veins as well as the size of the wing and the shape of its outline. The heritability under laboratory and field conditions was also estimated from the parameters generated. Multivariate analysis showed that wing morphology possessed sufficient differences to discriminate between the two species with a successful classification rate of 95-98% for females and 82-87% for males. The results of the autoclassification were confirmed by a cross-validation test for females (92-96%). Most measurements possessed significant natural heritability (a mean of 0.48 for D. mercatorum and 0.88 for D. paranaensis), indicating that the variation observed was related to differences in genes acting additively. The principal difference between the two species was in the placement of the posterior transverse wing vein. However, the pattern of morphological variation in the wings of both species was similar, possibly because of shared restrictions in wing development pathways.     

The effects of latitude,body size,and sexual selection on wing shape in a damselfly

Under natural selection, wing shape is expected to evolve to optimize flight performance. However, other selective factors besides flight performance may influence wing shape. One such factor could be sexual selection in wing sexual ornaments, which may lead to alternative variations in wing shape that are not necessarily related to flight performance. In the present study, we investigated wing shape variations in a calopterygid damselfly along a latitudinal gradient using geometric morphometrics. Both sexes show wing pigmentation, which is a known signal trait at intra‐ and interspecific levels. Wing shape differed between sexes and, within the same sex, the shape of the hind wing differed from the front wing. Latitude and body size explained a high percentage of the variation in wing shape for female front and hind wings, and male front wings. In male hind wings, wing pigmentation explained a high amount of the variation in wing shape. On the other hand, the variation in shape explained by pigmentation was very low in females. We suggest that the conservative morphology of front wings is maintained by natural selection operating on flight performance, whereas the sex‐specific differences in hind wings most likely could be explained by sexual selection. The observed sexual dimorphism in wing shape is likely a result of different sex‐specific behaviours. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 263–274.     

Genetic variation for the positioning of wing veins in Drosophila melanogaster

SUMMARY To define the components of variation for wing shape in Drosophila in relation to what is known about the developmental control of wing patterning, we have characterized shape variation in the wings of 12 randomly chosen highly inbred lines. Despite large differences in wing size between males and females, and between flies reared at 18°C or 25°C, wing shape is remarkably unaffected by these variables and is highly line specific. The shape of each intervein region of the wing appears to be independently regulated at the genetic level, consistent with the role of secreted growth factors in establishing the locations of wing veins. Sex and temperature were found to have different effects on cell number in two intervein regions, with the result that wing shape is to a large extent independent of cell density. Dietary cholesterol was also shown to affect the breadth of the central intervein region, consistent with an effect on the strength of Hedgehog signaling during wing development. We conclude that wing shape is under tighter genetic control than wing size, and hypothesize that this control is achieved in large part by gene activity at the level of wing vein determination and differentiation.     

Effect of different larval rearing temperatures on the productivity (Ro) and morphology of the malaria vector Anopheles superpictus Grassi (Diptera: Culicidae) using geometric morphometrics

Temperature affects both the biology and morphology of mosquito vectors. Geometric morphometrics is a useful new tool for capturing and analyzing differences in shape and size in many morphological parameters, including wings. We have used this technique for capturing the differences in the wings of the malaria vector Anopheles superpictus, using cohorts reared at six different constant temperatures (15°, 20°, 25°, 27°, 30°, and 35° C) and also searched for potential correlations with the life tables of the species. We studied wing shape in both male and female adults, using 22 landmarks on the wing in relation to ecological parameters, including the development rate. The ecological zero was calculated as 9.93° C and the thermal constant as 296.34 day‐degrees. The rearing temperature affects egg, larval, and pupal development and also the total time from egg to adult. As rearing temperatures increased, longevity decreased in both sexes. In An. superpictus, R_o value and productivity correlated with the statistically significant gradual deformations in the wing shape related to size in both sexes. These deformations directly linked to differences in immature rearing temperatures. Analysis using PCA and UPGMA phenograms showed that although wings of females became narrower dorsoventrally as the temperature increased, they became broader in males. Comparisons of the wing landmarks indicated the medial part of the wing was most affected by larval rearing temperatures, showing relatively more deformations. Algorithmic values of the life tables were determined in correlation with the results of geometric morphometrics. Comparisons of centroid sizes in the cohorts showed that overall wing size became smaller in both sexes in response to higher rearing temperatures.     

Consequences of outbreeding on phenotypic plasticity in Drosophila mercatorum wings

A multivariate morphometric investigation was conducted on wings of two parthenogenetic Drosophila mercatorum strains and offspring (F1) of crosses between these parthenogenetic strains with highly inbred sexual individuals of the same species. The parental flies and F1 offspring were reared at three different temperatures: 20, 25, or 28°C. This design allows a comparison of completely homozygous individuals (parental generation) with identical heterozygote offspring (F1), which makes an analysis of phenotypic plasticity of morphometric traits possible, without a potentially confounding effect of genotype-environment interactions, which can increase the phenotypic variability. The same pattern of phenotypic plasticity of wing size between the homozygous parental strains and the heterozygous offspring was found in both strains with an apparent heterotic effect for wing size in the F1 at 25°C. At 20 and 28°C flies from the parental generation had the biggest wings. Phenotypic plasticity of shape was found to be strain dependent. A reduced level of developmental instability (DI) was found in the F1 as compared to the parental strain only in strain 1 reared at 20°C for the wing size and 25°C for the wing shape. For all the other treatments higher DI was found in the F1 when the difference was significant, which is suggestive of outbreeding depression. These findings are difficult to interpret since an apparent heterotic effect of size at 25°C is accompanied by higher DI (though not significant in strain 2) and complex changes in wing shape. Hence, we cannot conclude whether outbreeding lowers or increases the capacity to respond to environmental change via plastic responses and via changes of the level of DI. The degree of change of phenotypic plasticity and DI is trait specific, depending on the environment and on the genotypes which are hybridizing. Kristian Krag and Hans Thomsen have contributed equally.     

Wing geometry of Phlebotomus stantoni and Sergentomyia hodgsoni from different geographical locations in Thailand

Geographic populations of the two main sandflies genera present in Thailand were studied for species and population identification. Size and shape of Phlebotomus stantoni and Sergentomyia hodgsoni from different island and mainland locations were examined by landmark-based geometric morphometrics. Intraspecific and interspecific wing comparison was carried out based on 12 anatomical landmarks. The wing centroid size of P. stantoni was generally larger than that of S. hodgsoni. Within both species, wings from the continent were significantly larger than those from island populations. Size variation could be significant between geographic locations, but could also overlap between genera. The wing venation geometry showed non-overlapping differences between two species. The within-species variation of geometric shape between different geographical locations was highly significant, but it could not interfere with the interspecies difference. The lack of species overlapping in shape, and the high discrimination between geographic populations, make geometric shape a promising character for future taxonomic and epidemiological studies.     

Insect wing shape evolution: independent effects of migratory and mate guarding flight on dragonfly wings

Although, in some insect taxa, wing shape is remarkably invariant, the wings of Anisopteran dragonflies show considerable variation among genera. Because wing shape largely determines the high energetic costs of flight, it may be expected that interspecific differences are partly due to selection. In the present study, we examined the roles of long-distance migration and high-manoeuvrability mate guarding in shaping dragonfly wings, using a phylogeny-based comparative method, and geometric morphometrics to quantify wing shape. The results obtained show that migration affects the shape of both front and hind wings, and suggest that mate guarding behaviour may also have an effect, especially on the front wing. These effects on front wing shape are at least partly independent. Our findings are interesting when compared with the geographically widespread and ecologically diverse dipterans Acalyptratae (including the genus Drosophila ). The wings in that group are similar in function and structure, but show strikingly low levels of interspecific variation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 362–372.     

Adaptation to different climates results in divergent phenotypic plasticity of wing size and shape in an invasive drosophilid

The phenotypic plasticity of wing size and wing shape of Zaprionus indianus was investigated in relation to growth temperature (17°C to 31°C) in two natural populations living under different climates, equatorial and subtropical. The two populations were clearly distinguished not only by their wing size (the populations from the colder climate being bigger in size), but also by the shape of the response curves to growth temperature i.e., their reaction norms. In this respect, the temperature at which the size of the wing was maximum was about 3°C higher in the equatorial population. Such a difference in size plasticity is already found in two other nonclosely related species, might be a general evolutionary pattern in drosophilids. Wing shape was investigated by calculating an ellipse included into the wing blade, then by considering the ratio of the two axes, and also by analysing the angular position of 10 wing-vein landmarks. For an overall shape index (ratio of the two axes of the ellipse), a regular and almost linear increase was observed with increasing temperature i.e., a more round shape at high temperatures. Wing shape was also analysed by considering the variations of the various angles according to temperature. A diversity of response curves was observed, revealing either a monotonous increase or decrease with increasing temperature, and sometimes a bell shape curve. An interesting conclusion is that, in most cases, a significant difference was observed between the two populations, and the difference was more pronounced at low temperatures. These angular variations are difficult to interpret in an evolutionary context. More comparative studies should be undertaken before reaching some general conclusions.     

Relationship between body size and flying-related structures in Neotropical social wasps (Polistinae,Vespidae, Hymenoptera)

Body size influences wing shape and associated muscles in flying animals which is a conspicuous phenomenon in insects, given their wide range in body size. Despite the significance of this, to date, no detailed study has been conducted across a group of species with similar biology allowing a look at specific relationship between body size and flying structures. Neotropical social vespids are a model group to study this problem as they are strong predators that rely heavily on flight while exhibiting a wide range in body size. In this paper we describe the variation in both wing shape, as wing planform, and mesosoma muscle size along the body size gradient of the Neotropical social wasps and discuss the potential factors affecting these changes. Analyses of 56 species were conducted using geometric morphometrics for the wings and lineal morphometrics for the body; independent contrast method regressions were used to correct for the phylogenetic effect. Smaller vespid species exhibit rounded wings, veins that are more concentrated in the proximal region, larger stigmata and the mesosoma is proportionally larger than in larger species. Meanwhile, larger species have more elongated wings, more distally extended venation, smaller stigmata and a proportionally smaller mesosoma. The differences in wing shape and other traits could be related to differences in flight demands caused by smaller and larger body sizes. Species around the extremes of body size distribution may invest more in flight muscle mass than species of intermediate sizes.     

Geographical and sexual variation of wing size in the monophagous flower-breeding species Drosophila flavopilosa

Flower samples of Cestrum parqui (Solanaceae) containing preadult forms of Drosophila flavopilosa were collected at four localities from the Maipo Valley in the Central zone of Chile (Lat. 33°40'S), one at sea level and the others at 300 m, 780 m and 1365 m of altitude. Only the adults which emerged after 18 days of permanency of the flowers in a chamber at 22°C were employed for wing analysis. Nine different measurements were made in the wings of 100 males and 100 females from each population. In males, a clear tendency of increasing wing length and width according to elevation above sea level was found. Females, however, exhibited a quite different type of variation; the larger and wider wings corresponding to the populations originated in the laces of intermediate elevation. As a result of the different pattern of wing variation in males and females, the sexual dimorphism was found to be significantly different between the studied populations. The results support the idea that males and females react in a different way to selective pressures affecting wing development.     

Heritability of Wing Morphology in a Natural Population of Drosophila gouveai

The natural and laboratory heritabilities of a series of parameters related to wing size and shape were estimated in a population of Drosophila gouveai (repleta group) under field and laboratory conditions. A morphometric analysis was done using 17 wing parameters related to wing landmark positions obtained using the method of the best adjustment of an ellipse to the wing edge. Three parameters (thetaA, thetaC and thetaD) showed highly significant heritability in the wild (average 0.61), whereas only wing size (W(SI)) had significant heritability in the laboratory (0.71). The additive genetic variance of most parameters was greater in the wild than in the laboratory. These results showed that some parameters possessed a substantial genetic additive component in their phenotypic variance, and that morphometric parameters of D. gouveai wings are appropriate quantitative markers for assessing morphological differentiation among populations.     

Age-related variation in wing shape of migratory and sedentary Blackcaps Sylvia atricapilla

In many passerines, juveniles have shorter and more rounded wings than adults. Given that (1) long and pointed wings improve endurance in migratory flights, (2) shorter and rounded wings improve manoeuvrability, and (3) juvenile birds are more vulnerable to predators than adults, it has been hypothesised that ontogenetic variation in wing shape results from a greater importance of predation avoidance relative to migration performance during the first year of life. If so, wing shape should not change with age in the absence of migration-related selection for longer and more pointed wings. We test this by studying the variation with respect to age in wing length and wing pointedness of migratory and sedentary Blackcaps wintering in southern Spain. Migratory Blackcaps had longer and more pointed wings than sedentary Blackcaps. Juveniles had shorter wings than adults in migratory populations, but not in sedentary populations. The variation with age in wing pointedness was less pronounced, and was found in migratory females only. These differences between the two traits could be related to a stronger selection for pointed wings than for longer wings with increasing distance of migration, and to an increased migratoriness of females in partially migratory Blackcap populations. We hypothesise that, in migratory Blackcaps, a shorter and more rounded wing in juveniles could be selected for if the decrease in predation rate compensated for the somewhat greater costs of the first migration attempt. On the other hand, there are no costs of migration in sedentary Blackcaps, which hence maintain a similar wing shape, giving high manoeuvrability, both as juveniles and as adults.     

Effect of fruit host on wing morphology in Drosophila suzukii (Diptera: Drosophilidae): A first view using geometric morphometrics

The invasive alien fruit pest Drosophila suzukii, (Matsumura 1931) causes economic loss in soft‐skinned fruit production across Europe. After its first detection in 2008, the species has successfully expanded to a wide geographic area and invaded new host plants in a relatively short period of time. The aim of the present study was to analyze the connection between food preferences as host specialization and the morphology of D. suzukii. Population morphological variation in wings was investigated in two different host fruits (grape and strawberry) in which economic damage has been recorded. The geometric morphometric results revealed two noticeable wing shape morphotypes in D. suzukii (i.e. vein configuration) between the grape and strawberry fruits. Flies reared in grapes had wider wings, whereas flies grown in strawberries had more narrow wings. These differences in morphotype could be explained by the effects of wing aerodynamics, which affect the strength of the wings in flight. This, in turn, can lead to better dispersion within the associated fruit host. These results confirm that this extremely invasive species, found worldwide, is successful at spreading in part because of its potential to adapt rapidly under different rearing conditions. Therefore, adaptive variations in the wing shape of D. suzukii can be used to differentiate populations based on food preference (e.g. soft fruits) and can serve as an additional tool for detecting different bioecological types of D. suzukii.     

Intercontinental effect on sexual shape dimorphism and allometric relationships in the beetle pest Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae)

Hind wing shape variation was examined in 686 adult Diabrotica virgifera virgifera collected from maize plants in Europe and the USA Corn Belt, using geometric morphometric techniques. Sexual dimorphism at an Intercontinental scale was assessed using canonical variates analysis, a multivariate statistical method used to find the shape characters that best distinguish among groups of specimens. Our results showed that each of the populations of D. v. virgifera investigated in this study showed high levels of sex based hind wing shape dimorphism. In particular a stronger and more obvious pattern of hind wing shape variation was found in the USA than in Europe. These results support previous studies on D. v. virgifera wing shape that show that female D. v. virgifera have more elongated wings than males. These differences raise the question of whether sexual dimorphism may be modulated by natural selection.     

Lack of response to artificial selection on developmental stability of partial wing shape components in Drosophila melanogaster

Developmental stability, the ability of organisms to buffer their developmental processes against developmental noise is often evaluated with fluctuating asymmetry (FA). Natural genetic variation in FA has been investigated using Drosophila wings as a model system and the recent estimation of the heritability of wing shape FA was as large as 20 %. Because natural genetic variation in wing shape FA was found to localize in a partial component of the wings, heritable variation in specific parts of the wings might be responsible for FA estimation based on the whole wing shape. In this study, we quantified the shape of three partial components of the wings, and estimated the heritability of the wing shape FA based on artificial selections. As a result, FA values for the partial wing shape components did not respond to artificial selections and the heritability scores estimated were very small. These results indicate that natural additive genetic variation in FA of partial wing components was very small compared with that in a complex wing trait.     

WITHIN- AND BETWEEN-GENERATION EFFECTS OF TEMPERATURE ON THE MORPHOLOGY AND PHYSIOLOGY OF DROSOPHILA MELANOGASTER

We investigated the effects of developmental and parental temperatures on several physiological and morphological traits of adult Drosophila melanogaster. Flies for the parental generation were raised at either low or moderate temperature (18°C or 25°C) and then mated in the four possible sex-by-parental temperature crosses. Their offspring were raised at either 18°C or 25°C and then scored as adults for morphological (dry body mass, wing size, and abdominal melanization [females only]), physiological (knock-down temperature, and thermal dependence of walking speed), and life history (egg size) traits. The experiment was replicated, and the factorial design allows us to determine whether and how paternal, maternal, and developmental temperatures (as well as offspring sex) influence the various traits. Sex and developmental temperature had major effects on all traits. Females had larger bodies and wings, higher knock-down temperatures, and slower speeds (but similar shaped performance curves) than males. Development at 25°C (versus at 18°C) increased knock-down temperature, increased maximal speed and thermal performance breadth, decreased the optimal temperature for walking, decreased body mass and wing size, reduced abdominal melanization, and reduced egg size. Parental temperatures influenced a few traits, but the effects were generally small relative to those of sex or developmental temperature. Flies whose mother had been raised at 25°C (versus at 18°C) had slightly higher knock-down temperature and smaller body mass. Flies whose father had been raised at 25°C had relatively longer wings. The effects of paternal, maternal, and developmental temperatures sometimes differed in direction. The existence of significant within- and between-generation effects suggests that comparative studies need to standardize thermal environments for at least two generations, that attempts to estimate “field” heritabilities may be unreliable for some traits, and that predictions of short-term evolutionary responses to selection will be difficult.     

Flies evolved small bodies and cells at high or fluctuating temperatures

Recent theory predicts that the sizes of cells will evolve according to fluctuations in body temperature. Smaller cells speed metabolism during periods of warming but require more energy to maintain and repair. To evaluate this theory, we studied the evolution of cell size in populations of Drosophila melanogaster held at either a constant temperature (16°C or 25°C) or fluctuating temperatures (16 and 25°C). Populations that evolved at fluctuating temperatures or a constant 25°C developed smaller thoraxes, wings, and cells than did flies exposed to a constant 16°C. The cells of flies from fluctuating environments were intermediate in size to those of flies from constant environments. Most genetic variation in cell size was independent of variation in wing size, suggesting that cell size was a target of selection. These evolutionary patterns accord with patterns of developmental plasticity documented previously. Future studies should focus on the mechanisms that underlie the selective advantage of small cells at high or fluctuating temperatures.