Cooperation between Drosophila flies in searching behavior

In Drosophila melanogaster food search behaviour, groups of flies swarm around and aggregate on patches of food. We wondered whether flies explore their environment in a cooperative way as interactions between individual flies within a population might influence the flies' ability to locate food sources. We have shown that the food search behavior in the fruit fly Drosophila is a two-step process. Firstly, 'primer' flies search the environment and randomly land on different food patches. Secondly, the remaining group of flies move to the most favorable food source and aggregate there. We call this a 'search–aggregation' cycle. Our data demonstrate that flies do not individually assess all available food resources. Rather, social interactions between flies appear to affect their choice of a specific food patch. A genetic analysis of this 'search–aggregation' behavior shows that flies carrying mutations in specific genes (for example, the dunce ( dnc ) gene which codes for a phosphodiesterase) were defective in this search–aggregation behavior when compared to normal flies. Future investigations of the neuronal signaling involved in this behavior will help us to understand the complexities of this aspect of Drosophila social behaviour.     

Effects of early adult experience on host selection in insects: Some experimental and theoretical results

A field experiment with Drosophila melanogasterrevealed that when flies encounter a particular food type soon after emergence, the probability of their subsequently being attracted to such a resource is increased. In this experiment, the length of time flies experienced their postemergence environments was under the control of the flies themselves. The experiment thus realistically mimicked one form of experiential effect that may be important in nature. A theoretical model is developed which shows that enhanced adult preferences for the types of resources fed on as larvae can substantially increase the degree of host-based genetic subdivision within a polyphagous population.     

A test of host specialization by insect vectors as a mechanism for reproductive isolation among entomophilous fungal species

Epichloë species are self incompatible (heterothallic) fungi that must be fertilized by spermatia from individuals of opposite mating type for successful sexual reproduction to occur. Female flies of the genus Botanophila act as vectors of the fungi by ingesting and defecating spermatia (gametes) onto fungal stromata (fruiting bodies) after oviposition. Larvae feed and develop on the stromata and thus maintain a symbiotic relationship with Epichloë fungi. We hypothesized that sole dependence on fertilized stromata as a food source would promote specialization by flies to single compatible host species and that this specialization would promote reproductive isolation among Epichloë species. Analysis of progeny of ascospores from experimental field plots in Zurich, Switzerland, indicated prevalence of specific matings between stromata of the same host, and thus was consistent with the hypothesis that flies are species-specific in their visitation behaviour. Genetic analyses of spermatia contained in the faeces of individual flies also gave some support for this hypothesis. We recovered spermatia of 4 different Epichloë species from fly faeces. Comparison of spermatia found in fly faeces to those available from stromata showed flies avoided Epichloë clarkii and may have preferred Epichloë typhina . Interestingly, these are the only two Epichloë species known to be interfertile with one another. Individual flies tended to carry spermatia predominantly from one fungal species. Thus, flies may adopt a type of "majoring" and "minoring" behaviour when visiting fungi. Yet, Botanophila flies are not monolectic and often visited all hosts that were available within screened cages. In addition to any reproductive isolation flies may provide to some fungal species, differences in competitiveness among spermatia of different species deposited on the same stroma may favor intraspecific matings.     

Effects of aggregation pheromone on individual behaviour and food web interactions: a field study on Drosophila

Abstract.  1. The effects of an aggregation pheromone on individual behaviour and food web interactions were investigated in two ecological communities, using Drosophila melanogaster and D. simulans as focal species.
2. Fruit substrates with aggregation pheromone were significantly more attractive to adult D. melanogaster and D. simulans than control fruit substrates, and the response was positively dose dependent. Competing species and natural enemies were also significantly attracted to substrates with the aggregation pheromone of D. melanogaster and D. simulans .
3. Significantly more eggs were deposited on pheromone-treated fruits than on control fruits, and the microdistribution of eggs within fruits was correlated to the microdistribution of the pheromone. The aggregation pheromone induced more females to share the breeding site.
4. The extremely high densities of fruit flies in the large aggregations appeared to reduce the oviposition rate of females. Physical interactions with conspecific and heterospecifics were frequently observed in the aggregations, and often led to patch leaving of the fruit flies.
5. Competition for food among larvae occurred at high densities and parasitism was density dependent. Aggregation pheromones can be directly responsible for these patterns through their effects on the con- and heterospecific behaviour.
6. The combined results show that aggregation pheromones affect a multitude of aspects in the ecology of interacting animals. The importance of incorporating the communication signals in ecological theory of aggregations is discussed.     

The interference of truncated with normal potassium channel subunits leads to abnormal behaviour in transgenic Drosophila melanogaster.

The Shaker locus of Drosophila melanogaster encodes a family of A-type potassium channel subunits. Shaker mutants behave as antimorphs in gene dosage tests. This behaviour is due to the production of truncated A-channel subunits. We propose that they interfere with the function of their normal counterpart by forming multimeric A-channel structures. This hypothesis was tested by constructing transgenic flies carrying a heat-inducible gene encoding a truncated A-type potassium channel subunit together with a normal wild type doses of A-type potassium channel subunits. The altered subunit leads at larval, pupal or adult stages to the transformation of wild type into Shaker flies. The transformed flies exhibited a heat-inducible abnormal leg shaking behaviour and a heat-inducible facilitated neurotransmitter release at larval neuromuscular junctions. By the overexpression of an aberrant A-channel subunit the normal behaviour of transgenic D. melanogaster can be altered in a predictable way.     

Social Environment Influences Performance in a Cognitive Task in Natural Variants of the Foraging Gene

In Drosophila melanogaster, natural genetic variation in the foraging gene affects the foraging behaviour of larval and adult flies, larval reward learning, adult visual learning, and adult aversive training tasks. Sitters (for ^s) are more sedentary and aggregate within food patches whereas rovers (for^R) have greater movement within and between food patches, suggesting that these natural variants are likely to experience different social environments. We hypothesized that social context would differentially influence rover and sitter behaviour in a cognitive task. We measured adult rover and sitter performance in a classical olfactory training test in groups and alone. All flies were reared in groups, but fly training and testing were done alone and in groups. Sitters trained and tested in a group had significantly higher learning performances compared to sitters trained and tested alone. Rovers performed similarly when trained and tested alone and in a group. In other words, rovers learning ability is independent of group training and testing. This suggests that sitters may be more sensitive to the social context than rovers. These differences in learning performance can be altered by pharmacological manipulations of PKG activity levels, the foraging (for) gene''s gene product. Learning and memory is also affected by the type of social interaction (being in a group of the same strain or in a group of a different strain) in rovers, but not in sitters. These results suggest that for mediates social learning and memory in D. melanogaster.     

Fitness components of Drosophila melanogaster developed on a standard laboratory diet or a typical natural food source

Drosophila melanogaster is often used as a model organism in evolutionary biology and ecophysiology to study evolutionary processes and their physiological mechanisms. Diets used to feed Drosophila cultures differ between laboratories and are often nutritious and distinct from food sources in the natural habitat. Here we rear D. melanogaster on a standard diet used in our laboratory and a field diet composed of decomposing apples collected in the field. Flies developed on these two diet compositions are tested for heat, cold, desiccation, and starvation resistance as well as developmental time, dry body mass and fat percentage. The nutritional compositions of the standard and field diets were analyzed, and discussed in relation to the phenotypic observations. Results showed marked differences in phenotype of flies from the two types of diets. Flies reared on the field diet are more starvation resistant and they are smaller, leaner, and have lower heat resistance compared to flies reared on the standard diet. Sex specific effects of diet type are observed for several of the investigated traits and the strong sexual dimorphism usually observed in desiccation resistance in D. melanogaster disappeared when rearing the flies on the field diet. Based on our results we conclude that care should be taken in extrapolating results from one type of diet to another and especially from laboratory to field diets.     

Attraction of Drosophila melanogaster males to food-related and fly odours

The fruit fly Drosophila melanogaster has become a model for olfaction and odour-mediated behaviour. In the wild, Drosophila flies aggregate on decaying fruit where they mate and oviposit and a strategy to find mates would be to locate fruit which has already been colonized by other flies. We therefore developed a bioassay to investigate attraction of males to food and fly odours. We showed that upwind flights are initiated by food odours. At shorter distances, males are attracted by volatiles produced by conspecifics. However, only odours produced by copulating flies attract males. This suggests either a synergistic effect of both male and female odours or changes in pheromone release during mating, that indicate the presence of sexually receptive females. Our findings demonstrate the essential role of food odours and pheromones for mate location in D. melanogaster.     

Host genetics and pathogen species modulate infection-induced changes in social aggregation behaviour

Identifying how infection modifies host behaviours that determine social contact networks is important for understanding heterogeneity in infectious disease dynamics. Here, we investigate whether group social behaviour is modified during bacterial infection in fruit flies (Drosophila melanogaster) according to pathogen species, infectious dose, host genetic background and sex. In one experiment, we find that systemic infection with four different bacterial species results in a reduction in the mean pairwise distance within infected female flies, and that the extent of this change depends on pathogen species. However, susceptible flies did not show any evidence of avoidance in the presence of infected flies. In a separate experiment, we observed genetic- and sex-based variation in social aggregation within infected, same-sex groups, with infected female flies aggregating more closely than infected males. In general, our results confirm that bacterial infection induces changes in fruit fly behaviour across a range of pathogen species, but also highlight that these effects vary between fly genetic backgrounds and can be sex-specific. We discuss possible explanations for sex differences in social aggregation and their consequences for individual variation in pathogen transmission.     

Heritable variation in the attraction of Drosophila melanogaster to fruit in the field

Drosophila melanogaster were released at a field site and captured with two types of fruit pulp. When flies were rereleased they were more likely to be captured with the same type of fruit on which they were initially captured. Progeny reared in the laboratory tended to be attracted to the same type of fruit as their parents in field tests with two fruit combinations (lemon-orange, lemon-apple) but not a third combination (apple-orange). However, lines selected in the laboratory for increased attraction to apples or oranges over 15 generations differed in their response to these fruit types in the field. This indicates heritable variation for attraction to natural resources under field conditions. Simulations suggest that genotypes differed substantially in their responses to fruit resources.     

Behavioural and chemosensory responses of the turnip root fly (Delia floralis) to glucosinolates

This study investigates the behavioural and neural mechanisms involved in the oviposition behaviour of the turnip root fly,Delia floralis (Fallen). Behavioural studies showed that glucosinolates modulated the oviposition behaviour of the flies on artificial leaves as well as the number of eggs laid in the soil at the base of these leaves. Electrophysiological responses to glucosinolates were obtained from type A and type D sensilla on the prothoracic and mesothoracic tarsi, as well as from the long contact sensilla on the labellum. The neural responses from these sensilla were positively correlated with the oviposition behaviour of the flies and with the number of eggs laid. Of the eleven glucosinolates tested in the behavioural and electrophysiological tests, the flies were most responsive to glucobrassicanapin, gluconapin and glucobrassicin. The type D tarsal sensilla were more responsive to the glucosinolates than either the type A tarsal sensilla or the labellar sensilla. The structure-activity investigations showed that slight modifications to the chemical composition of the glucosinolates resulted in changes in neural activity.     

Phenotypic plasticity,but not adaptive tracking,underlies seasonal variation in post‐cold hardening freeze tolerance of Drosophila melanogaster

In temperate regions, an organism's ability to rapidly adapt to seasonally varying environments is essential for its survival. In response to seasonal changes in selection pressure caused by variation in temperature, humidity, and food availability, some organisms exhibit plastic changes in phenotype. In other cases, seasonal variation in selection pressure can rapidly increase the frequency of genotypes that offer survival or reproductive advantages under the current conditions. Little is known about the relative influences of plastic and genetic changes in short‐lived organisms experiencing seasonal environmental fluctuations. Cold hardening is a seasonally relevant plastic response in which exposure to cool, but nonlethal, temperatures significantly increases the organism's ability to later survive at freezing temperatures. In the present study, we demonstrate seasonal variation in cold hardening in Drosophila melanogaster and test the extent to which plasticity and adaptive tracking underlie that seasonal variation. We measured the post‐cold hardening freeze tolerance of flies from outdoor mesocosms over the summer, fall, and winter. We bred outdoor mesocosm‐caught flies for two generations in the laboratory and matched each outdoor cohort to an indoor control cohort of similar genetic background. We cold hardened all flies under controlled laboratory conditions and then measured their post‐cold hardening freeze tolerance. Comparing indoor and field‐caught flies and their laboratory‐reared G1 and G2 progeny allowed us to determine the roles of seasonal environmental plasticity, parental effects, and genetic changes on cold hardening. We also tested the relationship between cold hardening and other factors, including age, developmental density, food substrate, presence of antimicrobials, and supplementation with live yeast. We found strong plastic responses to a variety of field‐ and laboratory‐based environmental effects, but no evidence of seasonally varying parental or genetic effects on cold hardening. We therefore conclude that seasonal variation in post‐cold hardening freeze tolerance results from environmental influences and not genetic changes.     

An analysis of genetic differentiation among assortatively mating Drosophila melanogaster in Zimbabwe

African Drosophila melanogaster populations, and those from Zimbabwe in particular, have attracted much interest recently. African flies differ genetically from 'cosmopolitan' populations and were found to exhibit discriminative mating behaviour against individuals from 'cosmopolitan' populations. It has therefore been proposed that Zimbabwean and some other African populations are in an 'incipient stage of speciation'. However, whether the mating behaviour is an effective barrier against gene flow from other populations, and whether intra-population genetic differentiation has already evolved in sympatry is not known. Here, we took a population-based approach to test whether the well-characterized mating type differences have resulted in a genome-wide differentiation at the population level. Using 122 polymorphic microsatellite loci mapping to the third chromosome, we demonstrate a significant genetic differentiation between Zimbabwean flies differing in their mating behaviour. We also provide evidence to suggest that this difference is unlikely to be attributable to population structure within Zimbabwe. However, the analysis of individual microsatellite loci did not indicate more loci differentiating these two groups than expected by chance. Our data suggest that the 'Z'-'M' mating behaviour is strong enough to result in a small but significant genetic differentiation. Thus, future studies based on a larger population sample of flies characterized for their mating behaviour and using more markers are expected to provide more information on the genetic basis of the mating traits in the Zimbabwe flies.     

Herbivore response to habitat manipulation with floral resources: a study of the cabbage root fly

Biological control of pest insects can be improved by providing natural enemies with additional food resources such as floral nectar within the production field. However, herbivores may also benefit from this practice. The aim of this 3‐year field study was to investigate if dill and buckwheat, aimed as food resources for natural enemies, could increase the densities of the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae), a severe pest on crucifers. Differences in egg density, numbers of pupae and sex ratio were compared between cabbage plots with or without flowers. Habitat manipulation by intercropping flowering plants with cabbage did not increase the overall D. radicum egg density in our 3‐year study, and there were no significant differences in egg numbers between treatments in any year. No effect on the fecundity of D. radicum was observed, most likely because of the high mobility and feeding behaviour of the female flies, combined with high abundance and diversity of other food sources around the fields during this period. Despite equal egg numbers, fewer pupae were found in plots with flowers than without in one of three studied years. This finding suggests that natural enemies attacking larvae and pupae of D. radicum were either more abundant or efficient in cabbage plots with flowers.     

GENETIC AND ENVIRONMENTAL DETERMINANTS OF FOOD PREFERENCE IN DROSOPHILA TRIPUNCTATA

Mark-release-recapture field experiments involving two isofemale strains of Drosophila tripunctata revealed that strain identity strongly and consistently affected the preferences of both males and females for mushrooms versus tomatoes. Females, but not males, showed an augmented preference for the type of food on which they had been kept prior to release. The behavior of F2 flies from reciprocal crosses between the two strains demonstrated that genetic variation for food preference is autosomal and largely additive. Because mating often occurs in the vicinity of food in the wild, positive assortative mating with respect to genes for food preference may lead to greater phenotypic variance in preference, which could increase the variety of food resources used by a population.     

Pre-mating isolation is determined by larval rearing substrates in cactophilicDrosophila mojavensis. II. Effects of larval substrates on time to copulation,mate choice and mating propensity

Summary It has been hypothesized that reproductive character displacement has evolved in mainland Sonora, Mexico populations of cactophilicD. mojavensis due to the presence of a sympatric sibling speciesD. arizonae. In laboratory tests using ancestral Baja California populations and derived, sympatric mainland populations, asymmetrical sexual isolation has been observed among populations ofD. mojavensis where mainland females discriminate against Baja males. Effects of different pre-adult rearing environments on adult mating behaviour were assessed by comparing fermenting cactus tissues like those used in nature for breeding with laboratory media because previous studies have employed synthetic growth media for fly growth and development. Significant behavioural isolation was evident in all cases when larvae were reared on laboratory food, but was non-significant when flies were reared on fermenting cactus, except for the cactus used by most mainland populations, consistent with previous studies. Time to copulation of Baja females was greater than mainland females over all substrates, but male time to copulation did not differ between populations. Time to copulation for both sexes was significantly greater when flies were reared on laboratory food with one exception. The degree of behavioural isolation was weakly correlated with time to copulation across food types (Spearman rank correlation = 0.58,p = 0.099). Therefore, use of laboratory media in this and previous studies exaggerated adult pre-mating isolation and time to copulation in comparison to natural breeding substrates. These experiments suggest that a change in host substrates by saprophagous insects (where chemical differences exist between hosts) may have subtle effects on mating behaviour in a manner which promotes low levels of sexual isolation as a by-product of their utilization of a particular substrate during larval development. ForD. mojavensis, these results suggest that over evolutionary time, radiation into a new environment (from Baja to the mainland) allowed utilization of new host plants that may have incidentally promoted the sexual isolation patterns that have been observed within this species.See Etges (1992) for the first paper in this series.     

‘Does my Diet Affect my Perfume?’ Identification and Quantification of Cuticular Compounds in Five Drosophila melanogaster Strains Maintained over 300 Generations on Different Diets

Cuticular hydrocarbons (CHCs) in Drosophila melanogaster represent the basis of chemical communication being involved in many important biological functions. The aim of this study was to characterize chemical composition and variation of cuticular profiles in five D. melanogaster strains. These strains were reared for approximately 300 generations on five diets: standard cornmeal medium and substrates prepared with apple, banana, tomato, and carrot. Differences in quantity and/or quality in CHCs were assumed as a result of activation of different metabolic pathways involved in food digestion and adaptations to the particular diet type. In total, independently of sex and strain, 66 chemical compounds were identified. In females of all strains, 60 compounds were identified, while, in males, 47 compounds were extracted. Certain new chemical compounds for D. melanogaster were found. MANOVA confirmed that CHC amounts significantly depend on sex and substrates, as well as on their interactions. Discriminant analysis revealed that flies belonging to ‘apple’ and ‘carrot’ strains exhibited the most noticeable differences in CHC repertoires. A non‐hydrocarbon pheromone, cis‐vaccenyl acetate (cVA) also contributed to the variation in the pheromone bouquet among the strains. Variability detected in CHCs and cVA may be used in the explanation of differences in mating behaviour previously determined in analyzed fly strains.     

A geomagnetic declination compass for horizontal orientation in fruit flies

The Earth's geomagnetic field (GMF) is known to act as a sensory cue for magnetoreceptive animals such as birds, sea turtles, and butterflies in long‐distance migration, as well as in flies, cockroaches, and cattle in short‐distance movement or body alignment. Despite a wealth of information, the way that GMF components are used and the functional modality of the magnetic sense are not clear. A GMF component, declination, has never been proven to be a sensory cue in a defined biological context. Here, we show that declination acts as a compass for horizontal food foraging in fruit flies. In an open‐field test, adopting the food conditioning paradigm, food‐trained flies significantly orientated toward the food direction under ambient GMF and under eastward‐turned magnetic field in the absence of other sensory cues. Moreover, a declination change within the natural range, by alteration only of either the east–west or north–south component of the GMF, produced significant orientation of the trained flies, indicating that they can detect and use the difference in these horizontal GMF components. This study proves that declination difference can be used for horizontal foraging, and suggests that flies have been evolutionarily adapted to incorporate a declination compass into their multi‐modal sensorimotor system.     

The evolutionary history of Drosophila buzzatii XXVII

The correlation between body size and longevity was tested in an Argentinian natural population of Drosophila buzzatii. Mean thorax length of flies newly emerging from rotting cladodes of Opuntia vulgaris was significantly smaller than that of two samples of flies caught at baits. The present results which might be interpreted as directional selection for longevity favoring larger flies are in agreement with previous results achieved in a Spanish natural population of D. buzzatii. Flies emerging from different substrates showed significant differences in thorax length, suggesting that an important fraction of phenotypic variance can be attributed to environmental variability. However, laboratory and field work in different populations of D. buzzatii showed a significant genetic component for thorax length variation.     

Ecological genetics of abdominal pigmentation in Drosophila falleni: a pleiotropic link to nematode parasitism

Drosophila falleni belongs to the quinaria species group, whose species vary considerably in patterns of wing and abdominal pigmentation. Drosophila falleni itself exhibits substantial variation among wild flies in abdominal spotting patterns. A selection experiment revealed that natural populations of D. falleni harbor high levels of genetic variation for spot number: in 10 generations of selection modal spot number within populations declined from 18 (the modal number in wild-caught females) to as low as zero. Rearing flies at different temperatures shows that some of the variation among wild flies is likely to reflect variation in the environmental conditions under which they developed. Fitness assays did not reveal any cost of reduced spot number with respect to development time, adult survival, or female fecundity. However, spotless flies were almost twice as susceptible to infection by the nematode parasite Howardula aoronymphium. Thus, selection exerted by nematode parasites may influence pigmentation patterns and other, genetically correlated traits in natural populations D. falleni.