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Offspring sex-ratios are stable across the life-course in Drosophila simulans

Within populations, adult sex ratios influence population growth and extinction risk, mating behaviors and parental care. Additionally, sex ratio adjustment can have pronounced effects on individual fitness. Accordingly, it is important that we understand how often, and why, offspring sex ratios deviate from parity. In Drosophila melanogaster, females appear to improve their fitness by producing fewer sons when paired with older males. However, facultative sex ratio adjustment in D. melanogaster is controversial, and our understanding of how sex ratio skew affects fitness is hampered by pronounced sexual conflict in this species. Additionally, it is unclear if maternal age or quality interact with paternal age to influence offspring sex ratios. Here, we test whether offspring sex ratios vary as a function of maternal quality, and maternal and paternal age in Drosophila simulans, a sister species of D. melanogaster that lacks overt sexual conflict. We find that offspring sex ratios are slightly male biased overall, but constant across the female life-course, and independent of female quality, or paternal age. To really understand if, how and when females skew offspring sex ratios, we need studies linking offspring sex ratios to male and female phenotypes that are predicted to shift optimal investment in sons and daughters.

Supplementary material 1 from: Abram PK, McPherson AE, Kula R, Hueppelsheuser T, Thiessen J, Perlman SJ, Curtis CI, Fraser JL, Tam J, Carrillo J, Gates M, Scheffer S, Lewis M, Buffington M (2020) New records of Leptopilina, Ganaspis, and Asobara species associated with Drosophila suzukii in North America, including detections of L. japonica and G. brasiliensis. Journal of Hymenoptera Research 78: 1-17. https://doi.org/10.3897/jhr.78.55026

Collection information for specimens reported in: New records of Leptopilina, Ganaspis, and Asobara species associated with Drosophila suzukii in North America, including detections of L. japonica and G. brasiliensis

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, in Drosophila melanogaster

Organisms living in seasonally variable environments utilize cues such as light and temperature to induce plastic responses, enabling them to exploit favorable seasons and avoid unfavorable ones. Local adapation can result in variation in seasonal responses, but the genetic basis and evolutionary history of this variation remains elusive. Many insects, including Drosophila melanogaster, are able to undergo an arrest of reproductive development (diapause) in response to unfavorable conditions. In D. melanogaster, the ability to diapause is more common in high latitude populations, where flies endure harsher winters, and in the spring, reflecting differential survivorship of overwintering populations. Using a novel hybrid swarm-based genome wide association study, we examined the genetic basis and evolutionary history of ovarian diapause. We exposed outbred females to different temperatures and day lengths, characterized ovarian development for over 2800 flies, and reconstructed their full phased genomes. We found that diapause scored at two different developmental cutoffs has modest heritability, and we identified hundreds of SNPs associated with each of the two phenotypes. Alleles associated with one of the diapause phenotypes tend to be more common at higher latitudes, but these alleles do not show predictable seasonal variation. The collective signal of many small-effect, clinally varying SNPs can plausibly explain latitudinal phenotypic variation seen in North America. SNPs associated with diapause do not exhibit signs of recent selective sweeps, but most are segregating at relatively high frequencies in Africa, suggesting that variation in diapause relies on ancestral polymorphisms. Finally, we utilized outdoor mesocosms to track diapause under natural conditions. We found that hybrid swarms reared outdoors evolved increased propensity for diapause in late fall, whereas indoor control populations experienced no such change. Our results indicate that diapause is a complex, quantitative trait with different evolutionary patterns across time and space.

opencc-by-4.0Apr 2020View details →

Experimental evolution of virulence and associated traits in a Drosophila melanogaster – Wolbachia symbiosis

Evolutionary theory predicts that vertically transmitted symbionts are selected for low virulence, as their fitness is directly correlated to that of their host. In contrast with this prediction, the Wolbachia strain wMelPop drastically reduces its Drosophila melanogaster host lifespan at high rearing temperatures. It is generally assumed that this feature is maintained because the D. melanogaster–wMelPop symbiosis is usually not exposed to environmental conditions in which the symbiont is virulent. To test this hypothesis, we submitted wMelPop-infected D. melanogaster lines to 17 generations of experimental evolution at a high temperature, while enforcing late reproduction. The fly survival was measured at different time points, as well as two traits that have been proposed to be causally responsible for wMelPop virulence: its relative density and the mean number of octomom copies present in its genome. We hypothesised that these conditions would select for a reduced wMelPop virulence, a reduced wMelPop density, and a reduced octomom copy number. Our results indicate that density, octomom copy number and virulence are correlated. However, contrary to our expectations, we could not detect any reduction in virulence during the course of evolution. We discuss the significance of our results with respect to the evolutionary causes of wMelPop virulence and propose that intra-host selection could explain this conundrum.

Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster

Stem cells fuel the development and maintenance of tissues. Many studies have addressed how local signals from neighboring niche cells regulate stem cell identity and their proliferative potential. However, the regulation of stem cells by tissue-extrinsic signals in response to environmental cues remains poorly understood. Here we report that efferent octopaminergic neurons projecting to the ovary are essential for germline stem cell (GSC) increase in response to mating in female Drosophila. The neuronal activity of the octopaminergic neurons is required for mating-induced GSC increase as they relay the mating signal from Sex peptide receptor-positive cholinergic neurons. Octopamine and its receptor Oamb are also required for mating-induced GSC increase via intracellular Ca2+ signaling. Moreover, we identified Matrix metalloproteinase-2 as a downstream component of the octopamine-Ca2+ signaling to induce GSC increase. Our study provides a mechanism describing how neuronal system couples stem cell behavior to environmental cues through stem cell niche signaling.

Data from: Testing the thermal limits: Non-linear reaction norms drive disparate thermal acclimation responses in Drosophila melanogaster

Critical thermal limits are important ecological parameters for studying thermal biology and for modelling species' distributions under current and changing climatic conditions (including predicting the risk of extinction for species from future warming). However, estimates of the critical thermal limits are biased by the choice of assay and assay conditions, which differ among studies. Furthermore, estimates of the potential for phenotypic plasticity (thermal acclimation) to buffer against future warming are usually based on single assay conditions and (usually linear) extrapolation from a few acclimation temperatures. We produced high resolution estimates of adult acclimation capacity for upper tolerance limits at different assay conditions (ramping rates and knock-down temperatures) using CTmax (dynamic) and knock-down (static) thermal assays in the model species Drosophila melanogaster. We found the reaction norms to be highly dependent on assay conditions. We confirmed that progressively lower ramping rates or higher knock-down temperatures led to overall lower tolerance estimates. More surprisingly, extended assays (lower ramping rates or lower knock-down temperatures) also led to increasingly non-linear reaction norms for upper thermal tolerance across adult acclimation temperatures. Our results suggest that the magnitude (capacity) and direction (beneficial or detrimental) of acclimation responses are highly sensitive to assay conditions. The results offer a framework for comparison of acclimation responses between different assay conditions and a potential for explaining disparate acclimation capacity theories. We advocate cautious interpretation of acclimation capacities and careful consideration of assay conditions, which should represent realistic environmental conditions based on species' ecological niches.

Data from: Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster

In Drosophila, long sperm are favoured in sperm competition based on the length of the female's primary sperm storage organ, the seminal receptacle (SR). This sperm-SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. Here, we explore the costs and benefits of long sperm and SR genotypes, both in the sex that carries them and in the sex that does not. We measured male and female fitness in inbred lines of D. melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs, or short SRs. We specifically asked: what are the costs and benefits of long sperm in males and long SRs in females? Furthermore, do genotypes that generate long sperm in males or long SRs in females impose a fitness cost on the opposite sex? Answers to these questions will address whether long sperm are an honest indicator of male fitness, if male post-copulatory success is associated with male pre-copulatory success, if female choice benefits females or is costly, and whether intra-genomic conflict could influence evolution of these traits. We found that both sexes have increased longevity in long sperm and long SR genotypes. Males, but not females, from long SR lines had higher fecundity. Our results suggest that sperm-SR coevolution is facilitated by both increased viability and indirect benefits of long sperm and SRs in both sexes.

Temperature-dependent competitive outcomes between the fruit flies Drosophila santomea and D. yakuba

We use these data to test whether temperature can indirectly affect the fitness of Drosophila santomea and D. yakuba by altering interspecific competitive outcomes. We show that, when raised in isolation, both D. santomea and D. yakuba display similar variation in relative fitness across temperatures of 18°C, 22°C, and 25°C. However, D. santomea has higher fitness than D. yakuba when experiencing interspecific competition at 18°C, while the inverse is true at 25°C. Patterns of fitness across thermal and competitive environments therefore indicate that the outcome of interspecific competition varies with temperature. We then use a 'coexistence' experiment to show that D. santomea is rapidly (within 8 generations) extirpated when maintained with D. yakuba at 25°C. By contrast, D. santomea remains as (or more) abundant than D. yakuba over the course of ~10 generations when maintained at 18°C. Results provide an example of how the thermal environment can affect interspecific competition and suggest that some species may become more prone to extinction under scenarios of climate change through indirect effects of the thermal environment on competitive advantages between species.

opencc-zeroOct 2020View details →

Drosophila SWR1 and NuA4 complexes are defined by DOMINO isoforms

Histone acetylation and deposition of H2A.Z variant are integral aspects of active transcription. In Drosophila, the single DOMINO chromatin regulator complex is thought to combine both activities via an unknown mechanism. Here we show that alternative isoforms of the DOMINO nucleosome remodeling ATPase, DOM-A and DOM-B, directly specify two distinct multi-subunit complexes. Both complexes are necessary for transcriptional regulation but through different mechanisms. The DOM-B complex incorporates H2A.V (the fly ortholog of H2A.Z) genome-wide in an ATP-dependent manner, like the yeast SWR1 complex. The DOM-A complex, instead, functions as an ATP-independent histone acetyltransferase complex similar to the yeast NuA4, targeting lysine 12 of histone H4. Our work provides an instructive example of how different evolutionary strategies lead to similar functional separation. In yeast and humans, nucleosome remodeling and histone acetyltransferase complexes originate from gene duplication and paralog specification. Drosophila generates the same diversity by alternative splicing of a single gene.

opencc-zeroOct 2020View details →

Raw data for Leigh et al 2020: Satyrization in Drosophila fruiflies

The satyr of Greek mythology was half-man, half-goat, with an animal persona signifying immoderate sexual appetites. In biology, satyrization is the disruption of reproduction in matings between closely-related species. Interestingly, its effects are often reciprocally asymmetric, manifesting more strongly in one direction of heterospecific mating than the other. Heterospecific matings are well known to result in female fitness costs due to the production of sterile or inviable hybrid offspring and can also occur due to reduced female sexual receptivity, lowering the likelihood of any subsequent conspecific matings. Here we investigated the costs and mechanisms of satyrization in the Drosophila melanogaster species subgroup of fruitflies. The results showed that D. simulans females experienced higher fitness costs from a loss of remating opportunites due to significantly reduced post-mating sexual receptivity, than D. melanogaster females, as a result of reciprocal heterospecific matings. Reciprocal tests of the effects of male reproductive accessory gland protein (Acp) injections on female receptivity in pairwise comparisons between D. melanogaster and five other species within the melanogaster species subgroup revealed significant post-mating receptivity asymmetries. This was due to variation in the effects of heterospecific Acps within species with which D. melanogaster can mate heterospecifically, and significant but non-asymmetric Acp effects in species with which it cannot. We conclude that asymmetric satyrization due to post-mating effects of Acps may be common among diverging and hybridising species. The findings are of interest in understanding the evolution of reproductive isolation and species divergence.

opencc-zeroNov 2020View details →

Sex-specific sterility caused by extreme temperatures is likely to create cryptic changes to the operational sex ratio in Drosophila virilis

Climate change is increasing the frequency and severity of short-term heat shocks that threaten the persistence of natural populations. The effect of thermal stress on natural selection is a common topic of debate, but high temperatures can also influence sexual selection. Typically, males and females of a species can survive at similar extreme temperatures, but males have been shown to lose fertility at lower temperatures than females. Here, we examine how a brief exposure of pupae to high temperatures in the fruit fly Drosophila virilis affects adult fertility in both males and females. We find strong sexual dimorphism in temperature-induced sterility. This has the potential to quickly and unpredictably create populations composed of mostly sterile males and fertile females, resulting in changes to the operational sex ratio (OSR). These disruptions are likely to be cryptic and difficult to measure in the wild, especially considering that males can eventually recover fertility and that sterile males of some species can still copulate. Changes to the OSR in this way are likely to influence sexual selection by favouring females that can discriminate between fertile and sterilised males, and possibly leading to female-female conflict over a limited pool of fertile males. Further research on how cryptic disruptions to the OSR affect sexual selection dynamics is critical for understanding the impact of environmental change on biodiversity.

opencc-zeroDec 2020View details →

Data from: Testing evolutionary explanations for the lifespan benefit of dietary restriction in fruit flies (Drosophila melanogaster)

Dietary restriction (DR), limiting calories or specific nutrients without malnutrition, extends lifespan across diverse taxa. Traditionally, this lifespan extension has been explained as a result of diet-mediated changes in the trade-off between lifespan and reproduction, with survival favoured when resources are scarce. However, a recently proposed alternative suggests that the selective benefit of the response to DR is the maintenance of reproduction. This hypothesis predicts that lifespan extension is a side effect of benign laboratory conditions, and DR individuals would be frailer and unable to deal with additional stressors, and thus lifespan extension should disappear under more stressful conditions. We tested this by rearing outbred female fruit flies (Drosophila melanogaster) on 10 different protein:carbohydrate diets. Flies were either infected with a bacterial pathogen (Pseudomonas entomophila), injured with a sterile pinprick or unstressed. We monitored lifespan, fecundity and measures of ageing. DR extended lifespan and reduced reproduction irrespective of injury and infection. Infected flies on lower protein diets had particularly poor survival. Exposure to infection and injury did not substantially alter the relationship between diet and ageing patterns. These results do not provide support for lifespan extension under DR being a side effect of benign laboratory conditions.

opencc-by-4.0Dec 2020View details →

Experimental warming influences species abundances in a Drosophila host community through direct effects on species performance rather than altered competition and parasitism

Current global warming trends are expected to have direct effects on species through their sensitivity to temperature, as well as on their biotic interactions, with cascading indirect effects on species, communities, and entire ecosystems. To predict the community-level consequences of global change we need to understand the relative roles of both the direct and indirect effects of warming. We used a laboratory experiment to investigate how warming affects a tropical community of three species of Drosophila hosts interacting with two species of parasitoids over a single generation. Our experimental design allowed us to distinguish between the direct effects of temperature on host species performance, and indirect effects through altered biotic interactions (competition among hosts and parasitism by parasitoid wasps). Although experimental warming significantly decreased parasitism for all host-parasitoid pairs, the effects of parasitism and competition on host communities did not vary across temperatures. Instead, effects on host relative abundances were species-specific, with one host species dominating the community at warmer temperatures, independently of parasitism and competition treatments. Our results show that temperature shaped a Drosophila host community directly through differences in species’ thermal performance, and not via its influences on biotic interactions.

opencc-zeroDec 2020View details →

Sexual selection on the genital lobes of male Drosophila simulans

Sexual selection is thought to be responsible for the rapid divergent evolution of male genitalia with several studies detecting multivariate sexual selection on genital form. However, in most cases, selection is only estimated during a single episode of selection, which provides an incomplete view of net selection on genital traits. Here we estimate the strength and form of multivariate selection on the genitalia arch of Drosophila simulans when mating occurs in the absence of a competitor and during sperm competition, in both sperm defence and offense roles (i.e. when mating first and last). We found that the strength of sexual selection on the genital arch was strongest during non-competitive mating and weakest during sperm offense. However, the direction of selection was similar across selection episodes with no evidence for antagonistic selection. Overall, selection was not particularly strong despite genitals clearly evolving rapidly in this species.

opencc-by-4.0Dec 2020View details →

Mating and survival of sterile Drosophila suzukii, in presence and absence of food

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is a widely distributed pest species of soft-skinned fruits. Recent studies suggest the use of Sterile Insect Technique (SIT) as a control method for this species, however, many are the factors that can impact effectiveness of a SIT program, including environmental condition. Thus, we aimed to verify the influence of temperature and relative humidity on mating and survival of fertile and sterile D. suzukii, when insects were food provided or deprived. Highest mating rates were obtained when food provided flies (either fertile or sterile) were exposed to 25 ºC or 81-100% relative humidity, while extreme temperatures (10 and 35 ºC) and low humidity (below 60%) impaired mating. Overall, mating rate among food deprived flies was low in all temperatures and humidity levels tested, but fertile insects were more prone to mate when compared to sterile flies. Survival was negatively influenced by high temperatures, low relative humidity and food deprivation. The information present in this study is useful to be considered for transport and release of sterile D. suzukii.

opencc-zeroJan 2021View details →

Sequencing data and normalized counts for tripartite RNAseq of Drosophila, Wolbachia, and SINV virus

Wolbachia is a maternally transmitted bacterium that manipulates arthropod and nematode biology in myriad ways. The Wolbachia strain colonizing Drosophila melanogaster creates sperm-egg incompatibilities and protects its host against RNA viruses, making it a promising tool for vector control. Despite successful trials using Wolbachia-transfected mosquitoes for Dengue control, knowledge of how Wolbachia and viruses jointly affect insect biology remains limited. Using the Drosophila melanogaster model, transcriptomics and gene expression network analyses revealed pathways with altered expression and splicing due to Wolbachia colonization and virus infection. Included are metabolic pathways previously unknown to be important for Wolbachia-host interactions. Additionally, Wolbachia-colonized flies exhibit a dampened transcriptomic response to virus infection, consistent with early blocking of virus replication. Finally, using Drosophila genetics, we show Wolbachia and expression of nucleotide metabolism genes have interactive effects on virus replication. Understanding the mechanisms of pathogen blocking will contribute to the effective development of Wolbachia-mediated vector control programs.

opencc-zeroJan 2021View details →

Phototactic choices of Drosophila melanogaster

When organisms' environmental conditions vary unpredictably in time, it can be advantageous for individuals to hedge their phenotypic bets. It has been shown that a bet-hedging strategy underlies the high inter-individual diversity of phototactic choice in Drosophila melanogaster. This study shows that fruit flies from a population living in a boreal and relatively unpredictable climate had more variable phototactic choices than fruit flies from a more stable tropical climate, consistent with bet-hedging theory. We experimentally show that phototactic variability of D. melanogaster is regulated by the neurotransmitter serotonin (5-HT), which acts as a suppressor of the variability of phototactic choices. When fed 5-HT precursor, boreal flies exhibited lower variability, and they were insensitive to 5-HT inhibitor. The opposite pattern was seen in the tropical flies. Thus, the reduction of 5-HT in fruit flies' brains may be the mechanistic basis of an adaptive bet-hedging strategy in a less predictable boreal climate.

opencc-zeroDec 2016View details →

Data from: Invasive Drosophila suzukii facilitates Drosophila melanogaster infestation and sour rot outbreaks in the vineyards

How do invasive pests affect interactions between members of pre-existing agrosystems? The invasive pest Drosophila suzukii is suspected to be involved in the aetiology of sour rot, a grapevine disease that otherwise develops following Drosophila melanogaster infestation of wounded berries. We combined field observations with laboratory assays to disentangle the relative roles of both Drosophila in disease development. We observed the emergence of numerous D. suzukii, but no D. melanogaster flies, from bunches that started showing mild sour rot symptoms days after field collection. However, bunches that already showed severe rot symptoms in the field mostly contained D. melanogaster. In the laboratory, oviposition by D. suzukii triggered sour rot development. An independent assay showed the disease increased grape attractiveness to ovipositing D. melanogaster females. Our results suggest that in invaded vineyards, D. suzukii facilitates D. melanogaster infestation and, consequently, favours sour rot outbreaks. Rather than competing with close species, the invader subsequently permits their reproduction in otherwise non-accessible resources and may cause more frequent, or more extensive, disease outbreaks.

opencc-zeroDec 2015View details →

Data from: Life history evolution and cellular mechanisms associated with increased size in high-altitude Drosophila

Understanding the physiological and genetic basis of growth and body size variation has wide-ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high-altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large-bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller-bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.