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Data from: "De novo transcriptome assembly of the mountain fly Drosophila nigrosparsa using short RNA-seq reads" in Genomic Resources Notes Accepted 1 August 2014-30 September 2014
Drosophila (Drosophila) nigrosparsa is a habitat specialist restricted to the European montane/alpine zone (Bächli 2008). Mountain biodiversity is considered highly vulnerable to ongoing climate warming (IPCC 2013), and organisms at high altitudes have only limited possibility to shift to cooler habitats at elevations above (Pertoldi & Bach 2007). For such species, rapid evolution may offer a solution for long-term survival. We are establishing D. nigrosparsa as a model system to test the extent and tempo of adaptive evolution under thermal stress in the laboratory. In this study, we used Illumina high-throughput sequencing to assemble the species' transcriptome using the pooled mRNA from 22 developmental and physiological stages.
Data from: Genetic perturbation of key central metabolic genes extends life span in Drosophila and affects response to dietary restriction
There is a connection between nutrient inputs, energy-sensing pathways, lifespan variation and aging. Despite the role of metabolic enzymes in energy homeostasis and their metabolites as nutrient signals, little is known about how their gene expression impacts lifespan. In this report, we use P-element mutagenesis in Drosophila to study the effect on lifespan of reductions in expression of seven central metabolic enzymes, and contrast the effects on normal diet and dietary restriction. The major observation is that for five of seven genes, the reduction of gene expression extends lifespan on one or both diets. Two genes are involved in redox balance, and we observe that lower activity genotypes significantly extend lifespan. The hexokinases also show extension of lifespan with reduced gene activity. Since both affect the ATP/ADP ratio, this connects with the role of AMP-activated protein kinase as an energy sensor in regulating lifespan and mediating caloric restriction. These genes possess significant expression variation in natural populations, and our experimental genotypes span this level of natural activity variation. Our studies link the readout of energy state with the perturbation of the genes of central metabolism and demonstrate their effect on lifespan.
Data from: Behavioral elements and sensory cues involved in sexual isolation between Drosophila melanogaster strains
Sensory cues exchanged during courtship are crucial for mate choice: if they show intraspecific divergence this may cause or reinforce sexual isolation between strains, ultimately leading to speciation. There is a strong asymmetric sexual isolation between Drosophila melanogaster females from Zimbabwe (Z) and males from all other populations (M). While M and Z flies of both sexes show different cuticular pheromones, this variation is only partly responsible for the intraspecific isolation effect. Male acoustic signals are also partly involved in sexual isolation. We examined strain-specific courtship behaviour sequences to determine which body parts and sensory appendages may be involved in sexual isolation. Using two strains representative of the Z- and M-types, we manipulated sensory cues and the social context; we then measured the consequence of these manipulations on courtship and copulation. Our data suggest that Z females mated best with males whose sensory characteristics matched those of Z males in both quantity and quality. M females were less choosy and much less influenced by the sensory and social contexts. Differences in emission and reception of sensory signals seen between Z and M flies may lead to the concerted evolution of multiple sensory channel, thereby shaping a population-specific mate recognition system.
Data from: Genetic correlations among developmental and contextual behavioral plasticity in Drosophila melanogaster
Correlations among traits, including behaviors, are important because traits that are genetically correlated may not evolve independently. Recently, behavioral correlations research has expanded to include correlations not only in mean-level behaviors, but also in behavioral plasticity, i.e., the degree to which individuals change their behavior in response to environmental stimuli. Positive correlations among behavioral plasticities would imply that individuals or genotypes that are behaviorally plastic in one way may also be plastic in other ways; negative correlations could imply tradeoffs. Here, we examine aversive odor conditioning (learning) at two time points, and plasticity in pupation site selection behavior across substrates, in a panel of Drosophila genotypes. These behaviors represent different types of behavioral plasticity: contextual plasticity describes behavioral responses to stimuli that are currently present, while developmental plasticity describes behavioral responses to remembered experiences with stimuli in the recent past. We find that learning scores and plasticity in pupation site selection behavior are positively genetically correlated, representing the first example of a genetic correlation between developmental and contextual plasticity. These findings imply that ecological and evolutionary theories focusing on variation in a single dimension of behavioral plasticity may be incomplete.
Data from: Analyzing negative feedback using a synthetic gene network expressed in the Drosophila melanogaster embryo
Background: A complex network of gene interactions controls gene regulation throughout development and the life of the organisms. Insights can be made into these processes by studying the functional interactions (or "motifs") which make up these networks. Results: We sought to understand the functionality of one of these network motifs, negative feedback, in a multi-cellular system. This was accomplished using a synthetic network expressed in the Drosophila melanogaster embryo using the yeast proteins Gal4 (a transcriptional activator) and Gal80 (an inhibitor of Gal4 activity). This network is able to produce an attenuation or shuttling phenotype depending on the Gal80/Gal4 ratio. This shuttling behavior was validated by expressing Gal3, which inhibits Gal80, to produce a localized increase in free Gal4 and therefore signaling. Mathematical modeling was used to demonstrate the capacity for negative feedback to produce these varying outputs. Conclusions: The capacity of a network motif to exhibit different phenotypes due to minor changes to the network in multi-cellular systems was shown. This work demonstrates the importance of studying network motifs in multi-cellular systems.
Strong and weak cross-sex correlations govern the quantitative-genetic architecture of social group choice in Drosophila melanogaster
<p><span><span><span><span><span><span><span><span><span><span><span>When genotypes differ in niche-constructing traits, genotypes are expected to differ in which environments they experience, providing a novel causal relationship between genotypes, environments, and behavior. Such genetic variation in niche construction (or, more precisely, environment construction) is predicted to be especially important for social environments, yet the quantitative-genetic parameters governing such variation is still poorly understood. Here, we examine genetic variation and cross-sex genetic correlations for social environment-constructing behaviors. We focus on whether genetic variation in patch use—the tendency to spend time near food patches where conspecifics may be present—and group-size preference—the specific group size chosen when individuals are affiliating—is correlated or decoupled across sexes in the fruit fly, <i>Drosophila melanogaster</i>. Across three choice treatments, we find genotype and sex differences in how much time individuals spend near patches, and which group sizes they prefer. We find that the genetic basis of patch use is strongly coupled across sexes, whereas the genetic basis of group-size preference is completely <i>de</i>coupled across sexes. We discuss how these findings augment and complicate our understanding of the evolutionary genetics of social behaviors.</span></span></span></span></span></span></span></span></span></span></span></p>
Data from: Islands of retroelements are major components of Drosophila centromeres
Centromeres are essential chromosomal regions that mediate kinetochore assembly and spindle attachments during cell division. Despite their functional conservation, centromeres are amongst the most rapidly evolving genomic regions and can shape karyotype evolution and speciation across taxa. Although significant progress has been made in identifying centromere-associated proteins, the highly repetitive centromeres of metazoans have been refractory to DNA sequencing and assembly, leaving large gaps in our understanding of their functional organization and evolution. Here, we identify the sequence composition and organization of the centromeres of Drosophila melanogaster by combining long-read sequencing, chromatin immunoprecipitation for the centromeric histone CENP-A, and high-resolution chromatin fiber imaging. Contrary to previous models that heralded satellite repeats as the major functional components, we demonstrate that functional centromeres form on islands of complex DNA sequences enriched in retroelements that are flanked by large arrays of satellite repeats. Each centromere displays distinct size and arrangement of its DNA elements but is similar in composition overall. We discover that a specific retroelement, G2/Jockey-3, is the most highly enriched sequence in CENP-A chromatin and is the only element shared among all centromeres. G2/Jockey-3 is also associated with CENP-A in the sister species Drosophila simulans, revealing an unexpected conservation despite the reported turnover of centromeric satellite DNA. Our work reveals the DNA sequence identity of the active centromeres of a premier model organism and implicates retroelements as conserved features of centromeric DNA.
Data from: Model-based comparisons of phylogeographic scenarios resolve the intraspecific divergence of cactophilic Drosophila mojavensis
The cactophilic fly Drosophila mojavensis exhibits considerable intraspecific genetic structure across allopatric geographic regions and shows associations with different host cactus species across its range. The divergence between these populations has been studied for more than 60 years, yet their exact historical relationships have not been resolved. We analysed sequence data from 15 intronic X-linked loci across populations from Baja California, mainland Sonora-Arizona and Mojave Desert regions under an isolation-with-migration model to assess multiple scenarios of divergence. We also compared the results with a pre-existing sequence dataset of 8 autosomal loci. We derived a population tree with Baja California placed at its base and link their isolation to Pleistocene climatic oscillations. Our estimates suggest the Baja California population diverged from an ancestral Mojave Desert/mainland Sonora-Arizona group around 230-270 Kya, while the split between the Mojave Desert and mainland Sonora-Arizona populations occurred one glacial cycle later, 117-135 Kya years ago. Although we found these three populations to be effectively allopatric, model ranking could not rule out the possibility of a low-level of gene flow between two of them. Finally, the Mojave Desert population showed a small effective population size, consistent with a historical population bottleneck. We show that model-based inference from multiple loci can provide accurate information on the historical relationships of closely related groups allowing us to set into historical context a classic system of incipient ecological speciation.
Data from: Heat tolerance in Drosophila subobscura along a latitudinal gradient: contrasting patterns between plastic and genetic responses
Susceptibility to global warming relies on how thermal tolerances respond to increasing temperatures through plasticity or evolution. Climatic adaptation can be assessed examining the geographic variation in thermal-related traits. We studied latitudinal patterns in heat tolerance in Drosophila subobscura reared at two temperatures. We used four static stressful temperatures to estimate the thermal death time curves (TDT), and two ramping assays with fast and slow heating rates. TDT curves allow estimating the critical thermal maximum CTmax, by extrapolating to the temperature that would knockdown the flies almost 'instantaneously', and the thermal sensitivity to increasing stressful temperatures. We found a positive latitudinal cline for CTmax, but no clinal pattern for knockdown temperatures estimated from the ramping assays. Although high-latitude populations were more tolerant to an acute heat stress, they were also more sensitive to prolonged exposure to less stressful temperatures, supporting a trade-off between acute and chronic heat tolerances. Conversely, developmental plasticity did not affect CTmax but increased the tolerance to chronic heat exposition. The patterns observed from the TDT curves help to understand why the relationship between heat tolerance and latitude depends on the methodology used and, therefore, these curves provide a more complete and reliable measurement of heat tolerance.
Data from: Association of polyandry and sex-ratio drive prevalence in natural populations of Drosophila neotestacea
Selfish genetic elements bias their own transmission to the next generation, even at the expense of the fitness of their carrier. Sex-ratio (SR) meiotic drive occurs when an X-chromosome causes Y-bearing sperm to die during male spermatogenesis, so that it is passed on to all of the male's offspring, which are all daughters. How SR is maintained as a stable polymorphism in the absence of genetic suppressors of drive is unknown. Here, we investigate the potential for the female remating rate to affect SR dynamics in natural populations, using the fly Drosophila neotestacea. In controlled laboratory conditions, females from populations where SR is rare mate more often than females from populations where SR is common. Furthermore, only when males mate multiply does the average fertility of SR males relative to wild-type males decrease to a level that can prevent SR from spreading. Our results suggest that differences in the female mating rate among populations may contribute to SR dynamics in the wild, and thus also affect the outcome of this intragenomic conflict. In line with this, we also present evidence of a localized population crash due to SR that may have resulted from habitat fragmentation along with a reduced mating rate.
Data from: A genomic reference panel for Drosophila serrata
Here we describe a collection of re-sequenced inbred lines of Drosophila serrata, sampled from a natural population situated deep within the species endemic distribution in Brisbane, Australia. D. serrata is a member of the speciose montium group whose members inhabit much of south east Asia and has been well studied for aspects of climatic adaptation, sexual selection, sexual dimorphism, and mate recognition. We sequenced 110 lines that were inbred via 17-20 generations of full-sib mating at an average coverage of 23.5x with paired-end Illumina reads. 15,228,692 biallelic SNPs passed quality control after being called using the Joint Genotyper for Inbred Lines (JGIL). Inbreeding was highly effective and the average levels of residual heterozygosity (0.86%) were well below theoretical expectations. As expected, linkage disequilibrium decayed rapidly, with r2 dropping below 0.1 within 100 base pairs. With the exception of four closely related pairs of lines which may have been due to technical errors, there was no statistical support for population substructure. Consistent with other endemic populations of other Drosophila species, preliminary population genetic analyses revealed high nucleotide diversity and, on average, negative Tajima's D values. A preliminary GWAS was performed on a cuticular hydrocarbon trait, 2-MeC28 revealing 4 SNPs passing Bonferroni significance residing in or near genes. One gene Cht9 may be involved in the transport of CHCs from the site of production (oenocytes) to the cuticle. Our panel will facilitate broader population genomic and quantitative genetic studies of this species and serve as an important complement to existing D. melanogaster panels that can be used to test for the conservation of genetic architectures across the Drosophila genus.
Data from: Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy
Field populations of arthropods are often polymorphic for Wolbachia but the factors maintaining intermediate Wolbachia frequencies are generally not understood. In Drosophila melanogaster, Wolbachia frequencies are highly variable across the globe. We document the persistence of a Wolbachia infection frequency cline in D. melanogaster populations from eastern Australia across at least 20 years, with frequencies generally high in the tropics but lower in cool temperate regions. The results are interpreted using a model of frequency dynamics incorporating cytoplasmic incompatibility, imperfect maternal transmission and Wolbachia effects on fitness. Clinal variation is less pronounced in eastern North America which may reflect annual recolonization at higher latitudes. Limited samples from Africa from latitudes matching our tropical and subtropical samples from Australia and North America show comparably high infection frequencies, but some equatorial samples show lower frequencies. Adult dormancy across cold periods may contribute to the Australian Wolbachia cline. Infected flies exposed to cold conditions for an extended period had reduced fecundity and viability, an effect not evident in unexposed controls. These fitness costs may contribute to the relatively low Wolbachia frequencies in Australian temperate areas; whereas different processes, including cytoplasmic incompatibility induced by young males, may contribute to higher frequencies in tropical locations.
Data from: Genomic conflict drives patterns of X-linked population structure in Drosophila neotestacea
Intra-genomic conflict has the potential to cause widespread changes in patterns of genetic diversity and genome evolution. In this study, we investigate the consequences of sex-ratio (SR) drive on the population genetic patterns of the X-chromosome in Drosophila neotestacea. An SR X-chromosome prevents the maturation of Y-bearing sperm during male spermatogenesis, and thus is transmitted to ~100% of the offspring, nearly all of which are daughters. Selection on the rest of the genome to suppress sex-ratio can be strong, and the resulting conflict over the offspring sex ratio can result in the accumulation of multiple loci on the X-chromosome that are necessary for expression of drive. We surveyed variation at 12 random X-linked microsatellites across 16 populations of D. neotestacea that range in SR frequency from 0-30%. First, every locus was differentiated between SR and wild-type chromosomes, and this drives genetic structure at the X-chromosome. Once the association with sex-ratio is accounted for, the patterns of differentiation among populations are similar to the autosomes. Second, within wild-type chromosomes the relative heterozygosity is reduced in populations with an increased prevalence of drive, and the heterozygosity of SR chromosomes is higher than expected based on its prevalence. The combination of the relatively high prevalence of SR drive and the structuring of polymorphism between the SR and wild-type chromosomes suggests that genetic conflict due to SR drive has had significant consequences on the patterns of X-linked polymorphism and thus also likely affects the tempo of X-chromosome evolution in D. neotestacea.
Data from: Individual inversions or their combinations: which is the main selective target in a natural population of Drosophila subobscura?
It is generally accepted that chromosomal inversions have been key elements in adaptation and speciation processes. In this context, D. subobscura has been, and still is, an excellent model species due to its rich chromosomal polymorphism. In this species, many analyses from natural populations have demonstrated the adaptive potential of individual inversions (and their overlapped combinations, the so called arrangements). However, little information is available on the evolutionary role of combinations generated by inversions located in homologous and non-homologous chromosomes. The aim of this research is to ascertain whether these combinations are also a target for natural selection. For this objective, we have studied the inversion composition of homologous and non-homologous chromosomes from a D. subobscura sample collected in a well-studied population, Mount Avala (Serbia). No significant deviation from H-W expectations was detected, and when comparing particular karyotypic combinations, likelihood ratios close to 1 were obtained. Thus, it seems that for each pair of homologous chromosomes inversions no deviation from randomness was detected. Finally, no linkage disequilibrium was observed between inversions located in different chromosomes of the karyotype. For all these reasons it can be assumed that, at the cytological level, the individual inversions rather than their combinations in different chromosomes are the main target of selection.
Data from: Genetic analysis of circadian responses to low frequency electromagnetic fields in Drosophila melanogaster
The blue-light sensitive photoreceptor cryptochrome (CRY) may act as a magneto-receptor through formation of radical pairs involving a triad of tryptophans. Previous genetic analyses of behavioral responses of Drosophila to electromagnetic fields using conditioning, circadian and geotaxis assays have lent some support to the radical pair model (RPM). Here, we describe a new method that generates consistent and reliable circadian responses to electromagnetic fields that differ substantially from those already reported. We used the Schuderer apparatus to isolate Drosophila from local environmental variables, and observe extremely low frequency (3 to 50 Hz) field-induced changes in two locomotor phenotypes, circadian period and activity levels. These field-induced phenotypes are CRY- and blue-light dependent, and are correlated with enhanced CRY stability. Mutational analysis of the terminal tryptophan of the triad hypothesised to be indispensable to the electron transfer required by the RPM reveals that this residue is not necessary for field responses. We observe that deletion of the CRY C-terminus dramatically attenuates the EMF-induced period changes, whereas the N-terminus underlies the hyperactivity. Most strikingly, an isolated CRY C-terminus that does not encode the Tryptophan triad nor the FAD binding domain is nevertheless able to mediate a modest EMF-induced period change. Finally, we observe that hCRY2, but not hCRY1, transformants can detect EMFs, suggesting that hCRY2 is blue light-responsive. In contrast, when we examined circadian molecular cycles in wild-type mouse suprachiasmatic nuclei slices under blue light, there was no field effect. Our results are therefore not consistent with the classical Trp triad-mediated RPM and suggest that CRYs act as blue-light/EMF sensors depending on trans-acting factors that are present in particular cellular environments.
Data from: Plasticity through canalization: the contrasting effect of temperature on trait size and growth in Drosophila
In most ectotherms, a reduction in developmental temperature leads to an increase in body size, a phenomenon known as the temperature size rule (TSR). In Drosophila melanogaster, temperature affects body size primarily by affecting critical size, the point in development when larvae initiate the hormonal cascade that stops growth and starts metamorphosis. However, while the thermal plasticity of critical size can explain the effect of temperature on overall body size, it cannot entirely account for the effect of temperature on the size of individual traits, which vary in their thermal sensitivity. Specifically, the legs and male genitalia show reduced thermal plasticity for size, while the wings show elevated thermal plasticity, relative to overall body size. Here, we show that these differences in thermal plasticity among traits reflect, in part, differences in the effect of temperature on the rates of cell proliferation during trait growth. Counterintuitively, the elevated thermal plasticity of the wings is due to canalization in the rate of cell proliferation across temperatures. The opposite is true for the legs. These data reveal that environmental canalization at one level of organization may explain plasticity at another, and vice versa.
Data from: Local and landscape-scale heterogeneity shape spotted wing drosophila (Drosophila suzukii) activity and natural enemy abundance: implications for trophic interactions
Like natural enemies, invasive polyphagous pests may respond positively to local and landscape-scale diversity, making them more serious challenges to sustainable management than specialists. Yet the current view of landscape effects on pests rarely considers perennial systems or polyphagous pests. We investigated Drosophila suzukii (SWD) and natural enemy distributions and trophic interactions in blueberry systems of the southeast US in relation to local management and landscape structure. Fields were nested in 1-km landscapes along gradients of crop and forest heterogeneity (landscape compositional diversity) and field border and crop border lengths (landscape configurational diversity). Yeast-sugar bait traps were used to collect SWD and canopy suction sampling for natural enemies. Management practices at the local scale did not influence SWD abundance, but natural enemy abundance was higher in organic systems and fields with vegetation present between rows. Landscape configurational diversity and greater proportion of non-cropping habitat promoted higher SWD populations. Natural enemy communities were composed of highly generalized species, and contrary to our predictions, we observed lower abundances in landscapes with higher proportion of non-cropping area. Few predators were detected to have fed on SWD, and communities were dominated by predators with low specialization on prey in blueberry. Our results indicate that local and landscape features in blueberry landscapes have differential effects on a polyphagous pest and generalist natural enemies. Our initial analysis of predator diets, using a metabarcoding approach, suggests spatial structure in specialization on prey with high diversity of prey in predators collected in forested margins.
Data from: Dynamics of the continent-wide spread of a Drosophila defensive symbiont
Facultative symbionts can represent important sources of adaptation for their insect hosts and thus have the potential for rapid spread. Drosophila neotestacea harbors a heritable symbiont, Spiroplasma, that confers protection against parasitic nematodes. We previously found a cline in Spiroplasma prevalence across central Canada, ending abruptly at the Rocky Mountains. Resampling these populations nine years later revealed that Spiroplasma had increased substantially across the region, resembling a Fisherian wave of advance. Associations between Spiroplasma infection and host mitochondrial DNA indicate that the increase was due to local increase of Spiroplasma-infected flies. Finally, we detected Spiroplasma west of the Rocky Mountains for the first time and showed that defense against nematodes occurs in flies with a western genetic background. Because nematode infection is common throughout D. neotestacea's range, we expect Spiroplasma to spread to the Pacific coast.
Data from: Stage-specific genotype-by-environment interactions for cold and heat hardiness in Drosophila melanogaster.
Environments often vary across a life cycle, imposing fluctuating natural selection across development. Such fluctuating selection can drive evolutionary responses specific to distinct life-history stages. However, selection and genetic variation, phenotypic plasticity, and their interaction (GxE), as well as genetic correlation across development dictate stage-specific evolution. Thus, quantifying genetic covariance of fitness-related traits and plasticity across development is vital to determine whether stage-specific adaptation occurs in nature. Additionally, the interaction of genetic variation and environmental plasticity (GxE) may be stage-specific, leading to a 3-way interaction between genotype, environment, and development or GxDxE. To test for these patterns in a natural system, we exposed larvae and adults of Drosophila melanogaster isogenic lines derived from a natural population to extreme heat and cold after developmental acclimation to cool (18°C) and warm (25°C) conditions and measured genetic variance for thermal hardiness. We detected significant GxE that was specific to larvae and adults for cold and heat hardiness (GxDxE), but no significant genetic correlation across development for either trait at either acclimation temperature. However, cross-development phenotypic correlations for acclimation responses suggest that plasticity itself may be developmentally constrained, though rigorously testing this hypothesis requires more experimentation. In general, we find evidence for thermal niche adaptation across development as larvae are more heat-hardy while adults are more cold-hardy. These results illustrate the potential for stage-specific adaptation within a complex life cycle and highlight the importance of measuring traits at appropriate developmental stages and environmental conditions when predicting evolutionary responses to changing climates.
Data from: The consequences of genetic variation in male sex peptide gene-expression levels for SP retention and egg laying in female Drosophila
The accessory gland proteins (Acps) that male Drosophila melanogaster produce and transfer to females during copulation are key to male and female fitness. One Acp, the sex peptide (SP), is largely responsible for a dramatic increase in female egg laying and decrease in female receptivity after copulation. While genetic variation in male SP expression levels correlate with refractory period duration in females, it is unknown whether male SP expression influences female egg laying or if any effect of SP is mediated by SP retention in the female reproductive tract. Here we measured the amount of SP retained in the female reproductive tract after mating and female egg laying after copulating with virgin males. We found no correlation between male SP expression levels and egg laying, or the amount of SP in the female reproductive tract after mating. Additionally, the amount of SP retained in the female did not influence egg laying. These finding suggests that additional factors, such as variation in other Acps, are important for the retention of SP in females and its quantitative effects on egg laying. It also shows that egg laying and refractory period response to SP is at least partially uncoupled.
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