Natural Populations Of Drosophila Research Articles

Demographic analyses of a new sample of haploid genomes from a Swedish population of Drosophila melanogaster

European and African natural populations of Drosophila melanogaster have been the focus of several studies aiming at inferring demographic and adaptive processes based on genetic variation data. However, in these analyses little attention has been given to gene flow between African and European samples. Here we present a dataset consisting of 14 fully sequenced haploid genomes sampled from a natural population from the northern species range (Umeå, Sweden). We co-analyzed this new data with an African population to compare the likelihood of several competing demographic scenarios for European and African populations and show that gene flow improves the fit of demographic models to data.

Parallel gene expression evolution in natural and laboratory evolved populations.

Ecological adaptation is frequently inferred by the comparison of natural populations from different environments. Nevertheless, inference of the selective forces suffers the challenge that many environmental factors covary. With well‐controlled environmental conditions, experimental evolution provides a powerful approach to complement the analysis of natural populations. On the other hand, it is apparent that laboratory conditions differ in many ways from natural environments, which raises the question as to what extent selection responses in experimental evolution studies can inform us about adaptation processes in the wild. In this study, we compared the expression profiles of replicated Drosophila melanogaster populations which have been exposed to two distinct temperature regimes (18/28 and 10/20°C) in the laboratory for more than 80 generations. Using gene‐wise differential expression analysis and co‐expression network analysis, we identified 541 genes and three coregulated gene modules that evolved in the same direction in both temperature regimes, and most of these changes probably reflect an adaptation to the space constraint or diurnal temperature fluctuation that is common in both selection regimes. In total, 203 genes and seven modules evolved temperature‐specific expression changes. Remarkably, we detected a significant overlap of these temperature‐adaptive genes/modules from experimental evolution with temperature‐adaptive genes inferred from natural Drosophila populations covering two different temperature clines. We conclude that well‐designed experimental evolution studies are a powerful tool to dissect evolutionary responses.

Predicting temperature mortality and selection in natural Drosophila populations.

Average and extreme temperatures will increase in the near future, but how such shifts will affect mortality in natural populations is still unclear. We used a dynamic model to predict mortality under variable temperatures on the basis of heat tolerance laboratory measurements. Theoretical lethal temperatures for 11 Drosophila species under different warming conditions were virtually indistinguishable from empirical results. For Drosophila in the field, daily mortality predicted from ambient temperature records accumulate over weeks or months, consistent with observed seasonal fluctuations and population collapse in nature. Our model quantifies temperature-induced mortality in nature, which is crucial to study the effects of global warming on natural populations, and analyses highlight that critical temperatures are unreliable predictors of mortality.

A Protamine Knockdown Mimics the Function of Sd in Drosophila melanogaster.

Segregation Distorter (SD) is an autosomal meiotic drive system found worldwide in natural populations of Drosophila melanogaster. This gene complex induces the preferential and nearly exclusive transmission of the SD chromosome in SD/SD+ males. This selfish propagation occurs through the interplay of the Sd locus, its enhancers and the Rsps locus during spermatid development. The key distorter locus, Sd, encodes a truncated but enzymatically active RanGAP (RanGTPase-activating protein), a key nuclear transport factor in the Ran signaling pathway. When encoded by Sd, RanGAP is mislocalized to the nucleus interior, which then traps Ran inside the nucleus and disrupts nuclear import. As a result of this aberrant nuclear transport, a process known as the histone-to-protamine transition that is required for proper spermatid condensation fails to occur in SD/SD+ males. In this process, sperm-specific protamine proteins enter the spermatid nucleus and replace the formerly chromatin-complexed histones. Previously, we have shown that mutations affecting nuclear import and export can enhance distortion in an SD background, thus verifying that a defect in nuclear transport is responsible for the unequal transmission of chromosomes. Herein, we show that specifically reducing protamines induces distortion in an SD background, verifying that protamines are transported via the RanGAP/GEF pathway and indicating that E(SD) plays a significant and unique role in the process of distortion.

Climate Factors and Wolbachia Infection Frequencies in Natural Populations of Drosophila melanogaster

The endosymbiotic bacteria Wolbachia are widespread in natural populations of Drosophila melanogaster, which is a cosmopolitan and synanthropic species. Various aspects of Wolbachia infection are studied in many arthropod species, including fruit flies. However, the influence of climatic factors on the level of Wolbachia infection in natural populations of fruit flies has not been studied in detail. The influence of mean temperature, precipitation, and potential evaporation was investigated on Wolbachia infection rates in ten D. melanogaster populations (collected in Europe) and newly obtained estimates were combined with the data from other studies for different continents and for different climatic zones (280 populations, 10 806 isofemale lines). The effect of climatic factors on the infection frequency was revealed. The highest infection rates are observed in the mean annual temperature range of 20–25°C, which corresponds to fly rearing conditions in the laboratory. The clinal distribution of Wolbachia infection rates in the Eurasian fruit fly populations was described. Logistic regression models showed that climatic factors have a stronger impact on bacterial infection rates within climatic zones rather than continents.

Live yeast in juvenile diet induces species-specific effects on Drosophila adult behaviour and fitness

The presence and the amount of specific yeasts in the diet of saprophagous insects such as Drosophila can affect their development and fitness. However, the impact of different yeast species in the juvenile diet has rarely been investigated. Here, we measured the behavioural and fitness effects of three live yeasts (Saccharomyces cerevisiae = SC; Hanseniaspora uvarum = HU; Metschnikowia pulcherrima = MP) added to the diet of Drosophila melanogaster larvae. Beside these live yeast species naturally found in natural Drosophila populations or in their food sources, we tested the inactivated “drySC” yeast widely used in Drosophila research laboratories. All flies were transferred to drySC medium immediately after adult emergence, and several life traits and behaviours were measured. These four yeast diets had different effects on pre-imaginal development: HU-rich diet tended to shorten the “egg-to-pupa” period of development while MP-rich diet induced higher larval lethality compared to other diets. Pre- and postzygotic reproduction-related characters (copulatory ability, fecundity, cuticular pheromones) varied according to juvenile diet and sex. Juvenile diet also changed adult food choice preference and longevity. These results indicate that specific yeast species present in natural food sources and ingested by larvae can affect their adult characters crucial for fitness.

A Drosophila melanogaster mitotype may have an adaptive meaning

Several different mitochondrial clades have been found in natural populations of Drosophila melanogaster. Most often, the difference is in single nucleotide substitutions, some of which are conservative. Some clades are rare, and others dominate. It has been reported that clade III dominates over clades V and VI in seven populations of D. melanogaster. We compared D. melanogaster strains with different mitotypes by locomotor activity (using TriKinetics Drosophila Activity Monitor), energy expenditure (by indirect calorimetry, based on measuring oxygen consumption) and life span (under extreme conditions at 29 °C). The nuclear genomes of these strains were aligned for several generations by backcrosses. According to our data, individuals with the mitotype from clade III had a higher level of locomotor activity and longer life span. In terms of energy expenditure, the strains studied did not differ. However, the same level of energy expenditure may be differently distributed between the state of activity and the state of rest or sleep. If the energy expenditure during the sleep in flies with different locomotor activity is the same, then an individual with the same overall energy expenditure can move a greater distance or be active longer. This can be interpreted as an advantage of the strain with the mitotype from clade III compared to the other two mitotypes studied. If individuals have different energy expenditure values at rest, the strains with lower energy expenditure at rest spend less energy during forced inactivity. In this case, the mitotype from clade III should also be advantageous. What nucleotide substitutions in the mitotype from clade III can provide an adaptive advantage is not clear yet. We assume that individuals with widespread clade М(III) may have adaptive advantages compared to other mitotypes due to their greater locomotor activity even with the same energy expenditure. Further studies are required, for mitotypes are polymorphic for single nucleotide polymorphism not only between but also within the clades.

Stage- and thermal-specific genetic architecture for preadult viability in natural populations of Drosophila melanogaster.

Studying the processes affecting variation for preadult viability is essential to understand the evolutionary trajectories followed by natural populations. This task requires focusing on the complex nature of the phenotype-genotype relationship by taking into account usually neglected aspects of the phenotype and recognizing the modularity between different ontogenetic stages. Here, we describe phenotypic variability for viability during the larval and pupal stages in lines derived from three natural populations of Drosophila melanogaster, as well as the variability for phenotypic plasticity and canalization at two different rearing temperatures. The results indicate that the three populations present significant phenotypic differences for preadult viability. Furthermore, distinct aspects of the phenotype (means, plasticity, canalization, plasticity of canalization) are affected by different genetic bases underlying changes in viability in a stage- and environment-specific manner. These findings explain the generalized maintenance of genetic variability for this fitness trait.

The spread of resistance to imidacloprid is restricted by thermotolerance in natural populations of Drosophila melanogaster.

Imidacloprid, the world's most used insecticide, has caused considerable controversy due to harmful effects on non-pest species and increasing evidence showing that insecticides have become the primary selective force in many insect species. The genetic response to insecticides is heterogeneous across populations and environments, leading to more complex patterns of genetic variation than previously thought. This motivated the investigation of imidacloprid resistance at different temperatures in natural populations of Drosophila melanogaster originating from four climate extremes replicated across two continents. Population and quantitative genomic analysis, supported by functional tests, have revealed a mixed genetic architecture to resistance involving major genes (Paramyosin and Nicotinic-Acetylcholine Receptor Alpha 3) and polygenes with a major trade-off with thermotolerance. Reduced genetic differentiation at resistance-associated loci indicated enhanced gene flow at these loci. Resistance alleles showed stronger evidence of positive selection in temperate populations compared to tropical populations in which chromosomal inversions In(2 L)t, In(3 R)Mo and In(3 R)Payne harbour susceptibility alleles. Polygenic architecture and ecological factors should be considered when developing sustainable management strategies for both pest and beneficial insects.

Study of Natural Genetic Variation in Early Fitness Traits Reveals Decoupling Between Larval and Pupal Developmental Time in Drosophila melanogaster

Characterizing the relationships between genotype and phenotype for developmental adaptive traits is essential to understand the evolutionary dynamics underlying biodiversity. In holometabolous insects, the time to reach the reproductive stage and pupation site preference are two such traits. Here we characterize aspects of the genetic architecture for Developmental Time (decomposed in Larval and Pupal components) and Pupation Height using lines derived from three natural populations of Drosophila melanogaster raised at two temperatures. For all traits, phenotypic differences and variation in plasticity between populations suggest adaptation to the original thermal regimes. However, high variability within populations shows that selection does not exhaust genetic variance for these traits. This could be partly explained by local adaptation, environmental heterogeneity and modifications in the genetic architecture of traits according to environment and ontogenetic stage. Indeed, our results show that the genetic factors affecting Developmental Time and Pupation Height are temperature-specific. Varying relationships between Larval and Pupal Developmental Time between and within populations also suggest stage-specific modifications of genetic architecture for this trait. This flexibility would allow for a somewhat independent evolution of adaptive traits at different environments and life stages, favoring the maintenance of genetic variability and thus sustaining the traits’ evolvabilities.

Drosophila melanogaster inhabiting northern regions of European Russia are infected with Wolbachia which adversely affects their life span

Wolbachia is a genus of bacteria causing intracellular infection in the natural populations of Drosophila melanogaster on all continents. In D. melanogaster , Wolbachia affects various life history traits, behaviour, sensitivity to stress and viral infection. The phenotypic effects of Wolbachia might evolve to promote its further spreading, increasing the interest in exploring the spread of Wolbachia , in particular, at the boundar­ies of the D. melanogaster habitat, in association with the effects on vital traits of host species. In this paper, we present data on the level of Wolbachia infection in two D. melanogaster populations from the northern regions of European Russia: Alexandrov (56.41° N, 38.72° E) and Valday (58.02° N, 33.24° E). The flies were collected in private apple gardens located in two small hamlets without supermarkets or fruit markets, from 2010 to 2015. The both populations demonstrated the same level of infection: in average, 69.7 % of the inbred lines (ILs) obtained from single females of the Alexan­drov population and 68.4 % of ILs obtained from single females of the Valday population. The infection rate varied from year to year showing a tendency to reduc­tion, its overall level being within the range previously observed in other habitats. Life spans were compared in sub-lines of the same IL, one infected with Wolbachia and the other treated with tetracycline healing this infection. In four out of five ILs, the lifespan of both males and females was severely affected by Wolbachia ; in different ILs, the mean life spans reduced from 1.8 to 5.4 times and from 1.4 to 2.4 times, respectively. Our results confirm that, despite D. melanogaster widespread distribution, the Wolbachia effect on their life span has been mostly negative.

Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster.

Animals are routinely colonized by microorganisms. Despite many studies documenting the microbial taxa associated with animals, the pattern and ecological determinants of among-animal variation in microbial communities are poorly understood. This study quantified the bacterial communities associated with natural populations of Drosophila melanogaster. Across five collections, each fly bore 16-78 OTUs, predominantly of the Acetobacteraceae, Lactobacillaceae, and Enterobacteriaceae. Positive relationships, mostly among related OTUs, dominated both the significant co-occurrences and co-association networks among bacteria, and OTUs with important network positions were generally of intermediate abundance and prevalence. The prevalence of most OTUs was well predicted by a neutral model suggesting that ecological drift and passive dispersal contribute significantly to microbiome composition. However, some Acetobacteraceae and Lactobacillaceae were present in more flies than predicted, indicative of superior among-fly dispersal. These taxa may be well-adapted to the Drosophila habitat from the perspective of dispersal as the principal benefit of the association to the microbial partners. Taken together, these patterns indicate that both stochastic processes and deterministic processes relating to the differential capacity for persistence in the host habitat and transmission between hosts contribute to bacterial community assembly in Drosophila melanogaster.

Effect of metabolites on stress, adaptation and longevity in laboratory populations of Drosophila flies

AbstractMetabolites like lipid and carbohydrate have significant roles on starvation, desiccation and longevity and differ in natural and laboratory populations of Drosophila. Five laboratory populations of Drosophila ananassae have been subjected to paraquat‐induced mortality and longevity, desiccation resistance, body size and ovariole number and tested for different metabolites (lipid, carbohydrate and water), fecundity and polymorphic chromosome inversions in each sex. Paraquat dose–response has clinal variation and means that paraquat mortality at different concentrations is significantly altered among males only. The overall mean ovariole number varies significantly (P ≪ 0.001) among different populations and one‐way ANOVA suggests significant variations (P ≪ 0.001) with mean fecundity and latitude. Only female longevity varies significantly among five different populations (P ≪ 0.001). Fecundity shows positive correlations with the longevity and suggests a possible role of different metabolites in keeping the cost effect. Two‐way ANOVA among mean water, lipid and carbohydrate contents in both sexes of different populations suggest significant differences among metabolites (P ≪ 0.001), between males and females (P ≪ 0.001, d.f. = 1) and for their interactions with each other (P ≪ 0.001) also. Significant differences are found for mean longevity, lipid and carbohydrate contents in both sexes of different populations in a two‐way ANOVA analysis (P ≪ 0.001), which suggests possible roles in their utilization at different levels during adaptation and stress. Longevity is affected significantly (P ≪ 0.001) by desiccation resistance also. Different chromosome inversions and their combinations show significant variations and sexual dimorphism with latitude and thorax length (P ≪ 0.001) and their roles are discussed in achieving adaptation, stress resistance and longevity.

Rapid seasonal evolution in innate immunity of wild Drosophila melanogaster.

Understanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes across a range of taxa. Here, we use immune defence in natural populations of Drosophila melanogaster to understand the rate of evolution in natural populations and the genetics underlying rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect along eastern North America (Massachusetts, Pennsylvania and Virginia). There are pronounced and repeatable changes in the immune response over the approximately 10 generations between spring and autumn collections, with a significant but less distinct difference observed among geographical locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles underlie the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defence in natural populations.

Inference of Transcription Factor Regulation Patterns Using Gene Expression Covariation in Natural Populations of Drosophila melanogaster

Gene regulatory networks control the complex programs that drive development. Deciphering the connections between transcription factors (TFs) and target genes is challenging, in part because TFs bind to thousands of places in the genome but control expression through a subset of these binding events. We hypothesize that we can combine natural variation of expression levels and predictions of TF binding sites to identify TF targets. We gather RNA-seq data from 71 genetically distinct F1 Drosophila melanogaster embryos and calculate the correlations between TF and potential target genes' expression levels, which we call "regulatory strength." To separate direct and indirect TF targets, we hypothesize that direct TF targets will have a preponderance of binding sites in their upstream regions. Using 14 TFs active during embryogenesis, we find that 12 TFs showed a significant correlation between their binding strength and regulatory strength on downstream targets, and 10 TFs showed a significant correlation between the number of binding sites and the regulatory effect on target genes. The general roles, e.g. bicoid's role as an activator, and the particular interactions we observed between our TFs, e.g. twist's role as a repressor of sloppy paired and odd paired, generally coincide with the literature.

The Genetic Architecture of Ovariole Number in Drosophila melanogaster: Genes with Major, Quantitative, and Pleiotropic Effects.

Ovariole number has a direct role in the number of eggs produced by an insect, suggesting that it is a key morphological fitness trait. Many studies have documented the variability of ovariole number and its relationship to other fitness and life-history traits in natural populations of Drosophila. However, the genes contributing to this variability are largely unknown. Here, we conducted a genome-wide association study of ovariole number in a natural population of flies. Using mutations and RNAi-mediated knockdown, we confirmed the effects of 24 candidate genes on ovariole number, including a novel gene, anneboleyn (formerly CG32000), that impacts both ovariole morphology and numbers of offspring produced. We also identified pleiotropic genes between ovariole number traits and sleep and activity behavior. While few polymorphisms overlapped between sleep parameters and ovariole number, 39 candidate genes were nevertheless in common. We verified the effects of seven genes on both ovariole number and sleep: bin3, blot, CG42389, kirre, slim, VAChT, and zfh1. Linkage disequilibrium among the polymorphisms in these common genes was low, suggesting that these polymorphisms may evolve independently.

Population Dynamics and Genetic Homogeneity in Natural Populations of Drosophila melanogaster from Faisalabad, Pakistan

Drosophila melanogaster has been considered an important model species to explore the patterns of diversity in natural populations. The current study was conducted to study population dynamics and genetic variability, gene flow and rate of migration in Faisalabad. The samples were collected from 17 different collection sites and cultured in the laboratory. The data for temperature and humidity were also recorded. It was observed that a decrease in temperature and increase in relative humidity caused an increase in population number and vice versa. Ten RAPD primers were used for PCR. Four primers were further selected on the basis of their efficiency and reproducibility. The number of amplification products varied from 4 to 10 with an average of 7.0 bands per primer. Mostly, all the samples showed monomorphic bands except for few samples from the south of the city. The allele and genotype frequencies were measured at each RAPD loci. Average observed heterozygosity (Ht 0.1886) and the genetic variation (G ST 0.129) showed that D. melanogaster natural populations had low level of genetic diversity. The dendrogram based on genetic similarities revealed three main groups of D. melanogaster populations. This pattern of genetic homogeneity due to low genetic variability in local populations was attributed to the gene flow with no genetic drift in D. melanogaster populations in Faisalabad.

Mid-day siesta in natural populations of D. melanogaster from Africa exhibits an altitudinal cline and is regulated by splicing of a thermosensitive intron in the period clock gene

BackgroundMany diurnal animals exhibit a mid-day ‘siesta’, generally thought to be an adaptive response aimed at minimizing exposure to heat on warm days, suggesting that in regions with cooler climates mid-day siestas might be a less prominent feature of animal behavior. Drosophila melanogaster exhibits thermal plasticity in its mid-day siesta that is partly governed by the thermosensitive splicing of the 3’-terminal intron (termed dmpi8) from the key circadian clock gene period (per). For example, decreases in temperature lead to progressively more efficient splicing, which increasingly favors activity over sleep during the mid-day. In this study we sought to determine if the adaptation of D. melanogaster from its ancestral range in the lowlands of tropical Africa to the cooler temperatures found at high altitudes involved changes in mid-day sleep behavior and/or dmpi8 splicing efficiency.ResultsUsing natural populations of Drosophila melanogaster from different altitudes in tropical Africa we show that flies from high elevations have a reduced mid-day siesta and less consolidated sleep. We identified a single nucleotide polymorphism (SNP) in the per 3’ untranslated region that has strong effects on dmpi8 splicing and mid-day sleep levels in both low and high altitude flies. Intriguingly, high altitude flies with a particular variant of this SNP exhibit increased dmpi8 splicing efficiency compared to their low altitude counterparts, consistent with reduced mid-day siesta. Thus, a boost in dmpi8 splicing efficiency appears to have played a prominent but not universal role in how African flies adapted to the cooler temperatures at high altitude.ConclusionsOur findings point towards mid-day sleep behavior as a key evolutionary target in the thermal adaptation of animals, and provide a genetic framework for investigating daytime sleep in diurnal animals which appears to be driven by mechanisms distinct from those underlying nighttime sleep.

Adaptive dynamics of cuticular hydrocarbons in Drosophila.

Cuticular hydrocarbons (CHCs) are hydrophobic compounds deposited on the arthropod cuticle that are of functional significance with respect to stress tolerance, social interactions and mating dynamics. We characterized CHC profiles in natural populations of Drosophila melanogaster at five levels: across a latitudinal transect in the eastern United States, as a function of developmental temperature during culture, across seasonal time in replicate years, and as a function of rapid evolution in experimental mesocosms in the field. Furthermore, we also characterized spatial and temporal changes in allele frequencies for SNPs in genes that are associated with the production and chemical profile of CHCs. Our data demonstrate a striking degree of parallelism for clinal and seasonal variation in CHCs in this taxon; CHC profiles also demonstrate significant plasticity in response to rearing temperature, and the observed patterns of plasticity parallel the spatiotemporal patterns observed in nature. We find that these congruent shifts in CHC profiles across time and space are also mirrored by predictable shifts in allele frequencies at SNPs associated with CHC chain length. Finally, we observed rapid and predictable evolution of CHC profiles in experimental mesocosms in the field. Together, these data strongly suggest that CHC profiles respond rapidly and adaptively to environmental parameters that covary with latitude and season, and that this response reflects the process of local adaptation in natural populations of D.melanogaster.

Pigmentation and fitness trade-offs through the lens of artificial selection.

Pigmentation is a classic phenotype that varies widely and adaptively in nature both within and among taxa. Genes underlying pigmentation phenotype are highly pleiotropic, creating the potential for functional trade-offs. However, the basic tenets of this trade-off hypothesis with respect to life-history traits have not been directly addressed. In natural populations of Drosophila melanogaster, the degree of melanin pigmentation covaries with fecundity and several other fitness traits. To examine correlations and potential trade-offs associated with variation in pigmentation, we selected replicate outbred populations for extreme pigmentation phenotypes. Replicate populations responded rapidly to the selection regime and after 100 generations of artificial selection were phenotyped for pigmentation as well as the two basic fitness parameters of fecundity and longevity. Our data demonstrate that selection on pigmentation resulted in a significant shift in both fecundity and longevity profiles. Selection for dark pigmentation resulted in greater fecundity and no pronounced change in longevity, whereas selection for light pigmentation decreased longevity but did not affect fecundity. Our results indicate the pleiotropic nature of alleles underlying pigmentation phenotype and elucidate possible trade-offs between pigmentation and fitness traits that may shape patterns of phenotypic variation in natural populations.