Natural Populations Of Drosophila Research Articles

P-M phenotypes and their correlation with longitude in natural populations of Drosophila melanogaster from Turkey

We analyzed the P-M gonadal dysgenesis characteristics and the molecular patterns of P and KP elements of 35 populations from distinct locations of Turkey and Cyprus to find out P element dynamics in natural populations of Drosophila melanogaster. The results of Gonadal dysgenesis (GD) tests showed a predominat M′ phenotype for this region. Besides Q populations were also found in less numbers. It was also noticed that there is a strong tendency for the presence of a Q type “buffer zone” in the Western part of Turkey. The variation in GD percentage (as a index for P element activity and susceptibility) observed among the populations did not show any clear relationship with some geoclimatic variables, but a significant correlation was found between longitude, and P element susceptibility. The P and KP element were also characterized by polymerase chain reaction amplification. The molecular analyses showed that all the populations examined have the entire of 1.15 kb KP element. The molecular patterns of KP elements have been found similar between the populations studied.

Natural variation in differentiated hemocytes is related to parasitoid resistance in Drosophila melanogaster

As a measure of parasitoid resistance, hemocyte load and encapsulation ability were measured in lines collected from natural populations of Drosophila melanogaster in Europe. Results show large geographic variation in resistance against the parasitoid wasp Asobara tabida among the field lines, but there was no clear correlation between resistance and total hemocyte load, neither before nor after parasitization. This was in contrast to the patterns that had been found in a comparison among species of Drosophila, where total hemocyte counts were positively correlated to encapsulation rates. This suggests that the mechanisms underlying between-species variation in parasitoid resistance do not extend to the natural variation that exists within a species. Although hemocyte counts did not correspond to encapsulation ability within D. melanogaster, the ratios of lamellocytes and crystal cells were very similar in lines with successful encapsulation responses. Apart from variation in the hemocytic response of the different hemocyte types, within-species variation was also observed for accurate targeting of the foreign body by the hemocytes. These results are discussed in the context of possible causes of variation in immune functions among natural populations.

Genomic variation in natural populations of Drosophila melanogaster.

This report of independent genome sequences of two natural populations of Drosophila melanogaster (37 from North America and 6 from Africa) provides unique insight into forces shaping genomic polymorphism and divergence. Evidence of interactions between natural selection and genetic linkage is abundant not only in centromere- and telomere-proximal regions, but also throughout the euchromatic arms. Linkage disequilibrium, which decays within 1 kbp, exhibits a strong bias toward coupling of the more frequent alleles and provides a high-resolution map of recombination rate. The juxtaposition of population genetics statistics in small genomic windows with gene structures and chromatin states yields a rich, high-resolution annotation, including the following: (1) 5'- and 3'-UTRs are enriched for regions of reduced polymorphism relative to lineage-specific divergence; (2) exons overlap with windows of excess relative polymorphism; (3) epigenetic marks associated with active transcription initiation sites overlap with regions of reduced relative polymorphism and relatively reduced estimates of the rate of recombination; (4) the rate of adaptive nonsynonymous fixation increases with the rate of crossing over per base pair; and (5) both duplications and deletions are enriched near origins of replication and their density correlates negatively with the rate of crossing over. Available demographic models of X and autosome descent cannot account for the increased divergence on the X and loss of diversity associated with the out-of-Africa migration. Comparison of the variation among these genomes to variation among genomes from D. simulans suggests that many targets of directional selection are shared between these species.

The SelfishSegregation DistorterGene Complex ofDrosophila melanogaster

Segregation Distorter (SD) is an autosomal meiotic drive gene complex found worldwide in natural populations of Drosophila melanogaster. During spermatogenesis, SD induces dysfunction of SD(+) spermatids so that SD/SD(+) males sire almost exclusively SD-bearing progeny rather than the expected 1:1 Mendelian ratio. SD is thus evolutionarily "selfish," enhancing its own transmission at the expense of its bearers. Here we review the molecular and evolutionary genetics of SD. Genetic analyses show that the SD is a multilocus gene complex involving two key loci--the driver, Segregation distorter (Sd), and the target of drive, Responder (Rsp)--and at least three upward modifiers of distortion. Molecular analyses show that Sd encodes a truncated duplication of the gene RanGAP, whereas Rsp is a large pericentromeric block of satellite DNA. The Sd-RanGAP protein is enzymatically wild type but mislocalized within cells and, for reasons that remain unclear, appears to disrupt the histone-to-protamine transition in drive-sensitive spermatids bearing many Rsp satellite repeats but not drive-insensitive spermatids bearing few or no Rsp satellite repeats. Evolutionary analyses show that the Sd-RanGAP duplication arose recently within the D. melanogaster lineage, exploiting the preexisting and considerably older Rsp satellite locus. Once established, the SD haplotype collected enhancers of distortion and suppressors of recombination. Further dissection of the molecular genetic and cellular basis of SD-mediated distortion seems likely to provide insights into several important areas currently understudied, including the genetic control of spermatogenesis, the maintenance and evolution of satellite DNAs, the possible roles of small interfering RNAs in the germline, and the molecular population genetics of the interaction of genetic linkage and natural selection.

A comparative analysis of the amounts and dynamics of transposable elements in natural populations of Drosophila melanogaster and Drosophila simulans

Genes are important in defining genetic variability, but they do not constitute the largest component of genomes, which in most organisms contain large amounts of various repeated sequences including transposable elements (TEs), which have been shown to account for most of the genome size. TEs contribute to genetic diversity by their mutational potential as a result of their ability to insert into genes or gene regulator regions, to promote chromosomal rearrangements, and to interfere with gene networks. Also, TEs may be activated by environmental stresses (such as temperature or radiation) that interfere with epigenetic regulation systems, and makes them powerful mutation agents in nature. To understand the relationship between genotype and phenotype, we need to analyze the portions of the genome corresponding to TEs in great detail, and to decipher their relationships with the genes. For this purpose, we carried out comparative analyses of various natural populations of the closely-related species Drosophila melanogaster and Drosophila simulans, which differ with regard to their TE amounts as well as their ecology and population size.

Accord insertion in the 5′ flanking region of CYP6G1 confers nicotine resistance in Drosophila melanogaster

What has driven the sweep of the Accord retrotransposon insertion allele of CYP6G1 in the natural populations of Drosophila melanogaster is unknown. Previous studies on the DDT selection hypothesis produced conflicting data. To reexamine the DDT selection hypothesis and search for alternative explanations, we conducted a series of correlation and genetic linkage experiments with eight D. melanogaster natural populations collected from California (CM1, CM2, CM3, and CM7) and Africa (AM2, AM3, AM4, AM7). Diagnostic PCR showed that CM1, CM2, CM7, and AM3 have the Accord insertion in the CYP6G1 locus, whereas the other four strains do not. RT-PCR analysis exhibits a 100% correlation between Accord insertion and CYP6G1 overexpression. However, among the four strains with Accord-mediated CYP6G1 overexpression only CM1 and CM7 are resistant to DDT, and the other two strains (CM2 and AM3), like the four Accord-free strains, are susceptible to DDT. By contrast, all the four strains with Accord-mediated CYP6G1 overexpression are resistant to nicotine, a plant allelochemical. Genetic crosses between DDT resistant and susceptible Accord-insertion strains, as well as crosses between Accord-insertion and Accord-free strains demonstrated that Accord insertion and CYP6G1 overexpression are genetically linked to nicotine resistance rather than DDT resistance. These results suggest that naturally-occurring allelochemicals such as nicotine are the initial driving force for the worldwide prevalence of the Accord insertion allele of CYP6G1 in D. melanogaster natural populations.

Partitioning sexual selection into its mating success and fertilization success components.

Postcopulatory sexual selection due to sperm competition and/or cryptic female choice has been documented in a diversity of taxonomic groups and is considered a pivotal component of sexual selection. Despite this apparent importance, the relative contribution of postcopulatory fertilization success to overall sexual selection has not yet been measured in any species. Here, we used a laboratory-adapted population of the promiscuous fruit fly Drosophila melanogaster to partition the variance in male reproductive success into mating success (a major component of precopulatory sexual selection) and fertilization success (a major component of postcopulatory sexual selection). We found that fertilization success contributed nearly as strongly as mating success to a male's net performance in sexual selection, but that most of this postcopulatory component was attributable to variation in male mating order (the tendency to be the last male to mate a female). After adjusting for mating order, only ≈2% of the residual variation in male reproductive success was attributable to differential fertilization success. We found no correlation between male mating success and fertilization success in this system. Unlike natural populations of Drosophila, our laboratory population is adapted to a semelparous lifecycle, so our findings will be most applicable to other promiscuous species with strong sperm precedence and one short breeding period per year or lifetime. In these species, fertilization success may have as much influence on male reproductive success as mating success, but the timing of mating (mating order) may be the predominant factor contributing to variation in fertilization success.

WOLBACHIA FROM NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER FROM UKRAINE

Проведено выявление и идентификация бактерий рода Wolbachia в природных популяциях Drosophila melanogaster Украины методом полимеразной цепной реакции c использованием специфических праймеров к фрагментам генов 16S рРНК и wsp, с последующим анализом прочтенных последовательностей. Эти бактерии обнаружены в 14 природных популяциях D. melanogaster Украины и относятся к штамму wMel.

The effect of mating on starvation resistance in natural populations of Drosophila melanogaster

In nature, behavioural and physiological processes involved in mating may entail different costs and benefits for males and females. However, it has been hypothesized that sexual interactions may have additional costs for Drosophila females like decrease in receptivity to remating and shortening of lifespan. During mating, males transfer seminal fluid proteins to females that exert severe physiological changes that may compromise female’s lifespan and reproductive success. However, under specific stressful environmental conditions that organisms usually face in nature, mating may also confer benefits to females. In the present work, we examine the effect of mating on starvation resistance in wild Drosophila melanogaster. We demonstrate that mated females derived from different geographic locations have the benefit of a greater starvation resistance as compared to virgin females. Even though mating status did not affect mean starvation resistance, we detected a strong genotype-specific effect in males. Beyond the obvious advantage of mating, our study reveals that mating might not be perilous for females, as envisaged by sexual conflict theories, but advantageous for flies exposed to shifts in environmental conditions. Thus, our results highlight the importance of studying other ecologically relevant traits that may contribute to the evolution of male–female interactions.

Genetic variation in heat-stress tolerance among South American Drosophila populations

Spatial or temporal differences in environmental variables, such as temperature, are ubiquitous in nature and impose stress on organisms. This is especially true for organisms that are isothermal with the environment, such as insects. Understanding the means by which insects respond to temperature and how they will react to novel changes in environmental temperature is important for understanding the adaptive capacity of populations and to predict future trajectories of evolutionary change. The organismal response to heat has been identified as an important environmental variable for insects that can dramatically influence life history characters and geographic range. In the current study we surveyed the amount of variation in heat tolerance among Drosophila melanogaster populations collected at diverse sites along a latitudinal gradient in Argentina (24°-38°S). This is the first study to quantify heat tolerance in South American populations and our work demonstrates that most of the populations surveyed have abundant within-population phenotypic variation, while still exhibiting significant variation among populations. The one exception was the most heat tolerant population that comes from a climate exhibiting the warmest annual mean temperature. All together our results suggest there is abundant genetic variation for heat-tolerance phenotypes within and among natural populations of Drosophila and this variation has likely been shaped by environmental temperature.

Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system.

Drosophila melanogaster is emerging as an important model of non-pathogenic host–microbe interactions. The genetic and experimental tractability of Drosophila has led to significant gains in our understanding of animal–microbial symbiosis. However, the full implications of these results cannot be appreciated without the knowledge of the microbial communities associated with natural Drosophila populations. In particular, it is not clear whether laboratory cultures can serve as an accurate model of host–microbe interactions that occur in the wild, or those that have occurred over evolutionary time. To fill this gap, we characterized natural bacterial communities associated with 14 species of Drosophila and related genera collected from distant geographic locations. To represent the ecological diversity of Drosophilids, examined species included fruit-, flower-, mushroom-, and cactus-feeders. In parallel, wild host populations were compared to laboratory strains, and controlled experiments were performed to assess the importance of host species and diet in shaping bacterial microbiome composition. We find that Drosophilid flies have taxonomically restricted bacterial communities, with 85% of the natural bacterial microbiome composed of only four bacterial families. The dominant bacterial taxa are widespread and found in many different host species despite the taxonomic, ecological, and geographic diversity of their hosts. Both natural surveys and laboratory experiments indicate that host diet plays a major role in shaping the Drosophila bacterial microbiome. Despite this, the internal bacterial microbiome represents only a highly reduced subset of the external bacterial communities, suggesting that the host exercises some level of control over the bacteria that inhabit its digestive tract. Finally, we show that laboratory strains provide only a limited model of natural host–microbe interactions. Bacterial taxa used in experimental studies are rare or absent in wild Drosophila populations, while the most abundant associates of natural Drosophila populations are rare in the lab.

Side effects of fungicides on the abundance and the species diversity of the natural populations of Drosophila and their hymenopterous parasitoids in orchards

Within entomophagous insects, hymenopterous parasitoids are important regulators of natural populations of insects including pests. Pesticide treatments are largely used in orchards for economic reasons. These treatments allow for greater productivity, but they may also impact upon non-target insect populations. Drosophila and their hymenopterous parasitoids are abundant in orchards and are not direct targets of pesticide treatments. In this work, natural populations of Drosophila and their parasitoids were monitored from June to November, and their abundance was reported from two types of orchards. One type was under conventional pesticide treatments, mostly fungicides (“Treated plot”), and the other was under low-input treatments (“Low-input plot”). Five Drosophila species and five parasitoid species were present in both types of orchards. A time effect on abundance was found with two peaks of abundance, one in August and the other in autumn (October), corresponding to a fluctuation of numbers depending on the availability of resources. When comparing insect abundance between the two types of plots, the abundance in the Treated plot was found to be lower than or equal to that in the Low-input plot. Furthermore, a significant decrease in the abundance of two scarce parasitoid species (Leptopilina heterotoma and Asobara tabida) that could lead to their disappearance was also observed. The results are discussed in the context of the diverse lethal and sub-lethal effects of pesticides on the development and reproduction of natural populations of insects and their importance as natural enemies.

Stability of genetic parameters in Drosophila melanogaster populations from Odesa

The dynamics of allele frequency of the carboxiesterase gene, the frequency of sex-linked lethal mutations, and recombination events in natural populations of Drosophila melanogaster from Odesa were studied. All studied estimates were shown to remain unchanged in June, July, and August during the 2009 collection season.

Positive correlation between malathion resistance and fecundity within natural populations of Drosophila melanogaster

The correlation between malathion resistance and fecundity was investigated in the fruit fly, Drosophila melanogaster. Previous studies have shown that insecticide resistance is negatively correlated with reproductive components in insects. To investigate this relationship, the fecundity (egg production) was determined in 2 natural and 2 esterase 6 (Est-6) marker populations (4016 and 4211) and malathion resistance levels (LC_{50}) were determined in the 4 populations of D. melanogaster. The resistance levels and Est-6 allozyme frequencies were compared to the results of 2 natural populations from Turkey (Antakya-Centre and Antalya-Serik) estimated in previous studies. In addition, malathion resistance levels (LC_{50}) were determined in 2 mutant populations using the paper contact method and the results were tested with Finney's probit analysis. In the bioassays, 4016 marker stock was more susceptible than the Antakya population and 4211 was more susceptible than the Serik population. The daily mean egg production numbers of females were calculated and compared using variance analysis (P < 0.05). The most productive population was found to be Antakya, followed by 4016, Serik, and 4211 populations, in decreasing order. These results indicate that malathion resistance is positively correlated with fecundity of 2 natural and 2 Est-6 marker stocks of D. melanogaster.

Copy-Number Variation: The Balance between Gene Dosage and Expression in Drosophila melanogaster

Copy-number variants (CNVs) reshape gene structure, modulate gene expression, and contribute to significant phenotypic variation. Previous studies have revealed CNV patterns in natural populations of Drosophila melanogaster and suggested that selection and mutational bias shape genomic patterns of CNV. Although previous CNV studies focused on heterogeneous strains, here, we established a number of second-chromosome substitution lines to uncover CNV characteristics when homozygous. The percentage of genes harboring CNVs is higher than found in previous studies. More CNVs are detected in homozygous than heterozygous substitution strains, suggesting the comparative genomic hybridization arrays underestimate CNV owing to heterozygous masking. We incorporated previous gene expression data collected from some of the same substitution lines to investigate relationships between CNV gene dosage and expression. Most genes present in CNVs show no evidence of increased or diminished transcription, and the fraction of such dosage-insensitive CNVs is greater in heterozygotes. More than 70% of the dosage-sensitive CNVs are recessive with undetectable effects on transcription in heterozygotes. A deficiency of singletons in recessive dosage-sensitive CNVs supports the hypothesis that most CNVs are subject to negative selection. On the other hand, relaxed purifying selection might account for the higher number of protein–protein interactions in dosage-insensitive CNVs than in dosage-sensitive CNVs. Dosage-sensitive CNVs that are upregulated and downregulated coincide with copy-number increases and decreases. Our results help clarify the relation between CNV dosage and gene expression in the D. melanogaster genome.

X-AUTOSOME INCOMPATIBILITIES IN DROSOPHILA MELANOGASTER: TESTS OF HALDANE'S RULE AND GEOGRAPHIC PATTERNS WITHIN SPECIES

Substantial genetic variation exists in natural populations of Drosophila melanogaster. This segregating variation includes alleles at different loci that interact to cause lethality or sterility (synthetic incompatibilities). Fitness epistasis in natural populations has important implications for speciation and the rate of adaptive evolution. To assess the prevalence of epistatic fitness interactions, we placed naturally occurring X chromosomes into genetic backgrounds derived from different geographic locations. Considerable amounts of synthetic incompatibilities were observed between X chromosomes and autosomes: greater than 44% of all combinations were either lethal or sterile. Sex-specific lethality and sterility were also tested to determine whether Haldane's rule holds for within-species variation. Surprisingly, we observed an excess of female sterility in genotypes that were homozygous, but not heterozygous, for the X chromosome. The recessive nature of these incompatibilities is similar to that predicted for incompatibilities underlying Haldane's rule. Our study also found higher levels of sterility and lethality for genomes that contain chromosomes from different geographical regions. These findings are consistent with the view that genomes are coadapted gene complexes and that geography affects the likelihood of epistatic fitness interactions.

A quantitative genetic study of starvation resistance at different geographic scales in natural populations ofDrosophila melanogaster

Food shortage is a stress factor that commonly affects organisms in nature. Resistance to food shortage or starvation resistance (SR) is a complex quantitative trait with direct implications on fitness. However, surveys of natural genetic variation in SR at different geographic scales are scarce. Here, we have measured variation in SR in sets of lines derived from nine natural populations of Drosophila melanogaster collected in western Argentina. Our study shows that within population variation explained a larger proportion of overall phenotypic variance (80%) than among populations (7·2%). We also noticed that an important fraction of variation was sex-specific. Overall females were more resistant to starvation than males; however, the magnitude of the sexual dimorphism (SD) in SR varied among lines and explained a significant fraction of phenotypic variance in all populations. Estimates of cross-sex genetic correlations suggest that the genetic architecture of SR is only partially shared between sexes in the populations examined, thus, facilitating further evolution of the SD.

Stage-Specific Effects of Candidate Heterochronic Genes on Variation in Developmental Time along an Altitudinal Cline of Drosophila melanogaster

BackgroundPreviously, we have shown there is clinal variation for egg-to-adult developmental time along geographic gradients in Drosophila melanogaster. Further, we also have identified mutations in genes involved in metabolic and neurogenic pathways that affect development time (heterochronic genes). However, we do not know whether these loci affect variation in developmental time in natural populations.Methodology/Principal FindingsHere, we constructed second chromosome substitution lines from natural populations of Drosophila melanogaster from an altitudinal cline, and measured egg-adult development time for each line. We found not only a large amount of genetic variation for developmental time, but also positive associations of the development time with thermal amplitude and altitude. We performed genetic complementation tests using substitution lines with the longest and shortest developmental times and heterochronic mutations. We identified segregating variation for neurogenic and metabolic genes that largely affected the duration of the larval stages but had no impact on the timing of metamorphosis.Conclusions/SignificanceAltitudinal clinal variation in developmental time for natural chromosome substitution lines provides a unique opportunity to dissect the response of heterochronic genes to environmental gradients. Ontogenetic stage-specific variation in invected, mastermind, cricklet and CG14591 may affect natural variation in development time and thermal evolution.

Transposable elements in natural populations ofDrosophila melanogaster

Transposable elements (TEs) are families of small DNA sequences found in the genomes of virtually all organisms. The sequences typically encode essential components for the replicative transposition sequences of that TE family. Thus, TEs are simply genomic parasites that inflict detrimental mutations on the fitness of their hosts. Several models have been proposed for the containment of TE copy number in outbreeding host populations such as Drosophila. Surveys of the TEs in genomes from natural populations of Drosophila have played a central role in the investigation of TE dynamics. The early surveys indicated that a typical TE insertion is rare in a population, which has been interpreted as evidence that each TE is selected against. The proposed mechanisms of this natural selection are reviewed here. Subsequent and more targeted surveys identify heterogeneity among types of TEs and also highlight the large role of homologous and possibly ectopic crossing over in the dynamics of the Drosophila TEs. The recent discovery of germline-specific RNA interference via the piwi-interacting RNA pathway opens yet another interesting mechanism that may be critical in containing the copy number of TEs in natural populations of Drosophila. The expected flood of Drosophila population genomics is expected to rapidly advance understanding of the dynamics of TEs.

Genotype and Gene Expression Associations with Immune Function in Drosophila

It is now well established that natural populations of Drosophila melanogaster harbor substantial genetic variation associated with physiological measures of immune function. In no case, however, have intermediate measures of immune function, such as transcriptional activity of immune-related genes, been tested as mediators of phenotypic variation in immunity. In this study, we measured bacterial load sustained after infection of D. melanogaster with Serratia marcescens, Providencia rettgeri, Enterococcus faecalis, and Lactococcus lactis in a panel of 94 third-chromosome substitution lines. We also measured transcriptional levels of 329 immune-related genes eight hours after infection with E. faecalis and S. marcescens in lines from the phenotypic tails of the test panel. We genotyped the substitution lines at 137 polymorphic markers distributed across 25 genes in order to test for statistical associations among genotype, bacterial load, and transcriptional dynamics. We find that genetic polymorphisms in the pathogen recognition genes (and particularly in PGRP-LC, GNBP1, and GNBP2) are most significantly associated with variation in bacterial load. We also find that overall transcriptional induction of effector proteins is a significant predictor of bacterial load after infection with E. faecalis, and that a marker upstream of the recognition gene PGRP-SD is statistically associated with variation in both bacterial load and transcriptional induction of effector proteins. These results show that polymorphism in genes near the top of the immune system signaling cascade can have a disproportionate effect on organismal phenotype due to the amplification of minor effects through the cascade.