Dissection of Complex, Fitness-Related Traits in Multiple Drosophila Mapping Populations Offers Insight into the Genetic Control of Stress Resistance.

We leverage two complementary Drosophila melanogaster mapping panels to genetically dissect starvation resistance-an important fitness trait. Using >1600 genotypes from the multiparental Drosophila Synthetic Population Resource (DSPR), we map numerous starvation stress QTL that collectively explain a substantial fraction of trait heritability. Mapped QTL effects allowed us to estimate DSPR founder phenotypes, predictions that were correlated with the actual phenotypes of these lines. We observe a modest phenotypic correlation between starvation resistance and triglyceride level, traits that have been linked in previous studies. However, overlap among QTL identified for each trait is low. Since we also show that DSPR strains with extreme starvation phenotypes differ in desiccation resistance and activity level, our data imply multiple physiological mechanisms contribute to starvation variability. We additionally exploited the Drosophila Genetic Reference Panel (DGRP) to identify sequence variants associated with starvation resistance. Consistent with prior work these sites rarely fall within QTL intervals mapped in the DSPR. We were offered a unique opportunity to directly compare association mapping results across laboratories since two other groups previously measured starvation resistance in the DGRP. We found strong phenotypic correlations among studies, but extremely low overlap in the sets of genomewide significant sites. Despite this, our analyses revealed that the most highly associated variants from each study typically showed the same additive effect sign in independent studies, in contrast to otherwise equivalent sets of random variants. This consistency provides evidence for reproducible trait-associated sites in a widely used mapping panel, and highlights the polygenic nature of starvation resistance.

Toxicity of three aphicides to the generalist predators Chrysoperla carnea (Neuroptera: Chrysopidae) and Orius insidiosus (Hemiptera: Anthocoridae).

Recent widespread infestations of the invasive sugarcane aphid, Melanaphis sacchari (Zehntner) (Hemiptera: Aphididae), in sorghum fields in the southern USA have created demand for insecticides that will provide effective control of sugarcane aphid, while conserving those beneficial species that contribute to biological control of the pest. We tested the susceptibility of both adult and immature stages of two aphid predators, the green lacewing, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), and the insidious flower bug, Orius insidiosus (Say) (Hemiptera: Anthocoridae), to three aphicides, flonicamid, sulfoxaflor and flupyradifurone. Flonicamid was innocuous to both species regardless of life stage or route of exposure. Lacewing adults were more susceptible to sulfoxaflor and flupyradifurone than were larvae, and had higher mortality when fed contaminated honey solution than when contacting residues on an inert surface. When laid in sunflower stems treated with these two materials, eggs of O. insidiosus hatched successfully, but nymphs experienced significant mortality when exposed to treated stems, likely due to phytophagous behavior that resulted in some insecticide ingestion. Despite these impacts, we conclude that both sulfoxaflor and flupyradifurone are likely to be relatively innocuous in comparison to more broad-spectrum insecticides and are thus potentially compatible with biological control and overall management of M. sacchari in grain sorghum.

Relative Toxicity of Two Aphicides to Hippodamia convergens (Coleoptera: Coccinellidae): Implications for Integrated Management of Sugarcane Aphid, Melanaphis sacchari (Hemiptera: Aphididae).

Flupyradifurone and sulfoxaflor present novel insecticide chemistries with particular efficacy against aphids, and the recent emergence of sugarcane aphid, Melanaphis sacchari (Zehntner), as a pest of sorghum in the United States has resulted in their widespread use. We examined their toxicity to Hippodamia convergens Guerin-Meneville, an important aphid biocontrol agent. We exposed beetles to topical applications of the field rate (FR) of these insecticides, fed them contaminated food (eggs of Ephestia kuehniella Zeller), and gave first-instar larvae 24-h exposures to leaf residues. More than half of fourth-instar larvae receiving topical applications of sulfoxaflor at FR survived, whereas flupyradifurone at 0.1× FR caused 90% mortality. Adults survived topical treatments better than larvae and without measurable mortality, except flupyradifurone at FR, which killed more than 80% of beetles. Survivors of all treatments had fertility similar to controls, whether treated as larvae or adults. Ingestion of contaminated food caused significant mortality in all treatments (15-40% for adults and 55-85% for larvae), with no significant differences between insecticides at FR. Leaf residues of sulfoxaflor at 1.0 and 2.0× FR caused approximately 60 and 80% mortality of first instars, respectively, whereas flupyradifurone at 0.1 and 1.0× FR caused > 90% mortality. Although sulfoxaflor was less toxic to H. convergens than flupyradifurone, the tested FR of flupyradifurone has now been reduced by half. We conclude that neither insecticide appears as toxic as other nicotinic acetylcholine receptor agonists, and that both materials are compatible with integrated pest management programs for M. sacchari.

Extending the "Ecology of Fear" Beyond Prey: Reciprocal Nonconsumptive Effects Among Competing Aphid Predators.

Nonconsumptive effects of predators on prey are well known, but similar effects among competing predators are not. Aphidophagous insect larvae are notorious for cannibalism and intraguild predation, as they compete for aggregated but ephemeral prey. We tested for indirect effects of competitors on the development of Coleomegilla maculata DeGeer and Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae), and a green lacewing, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), with all larvae reared on eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Control larvae were reared singly, while treatment larvae were reared pairwise, with either a conspecific or heterospecific, in partitioned Petri dishes that allowed the passage of chemical cues. Larvae of C. maculata, a dietary generalist, appeared stressed by the presence of competing larvae, whether con- or heterospecific, and suffered fitness costs (longer pupation times, lower male adult mass). In contrast, H. convergens and C. carnea, both aphid specialists, responded to competing larvae with accelerated development, and without any apparent costs in terms of adult size or reproductive performance. Adult C. carnea in some treatments were heavier than solitary controls, suggesting a higher consumption rate by the induced phenotype, and those exposed to H. convergens began oviposition earlier. Thus, the phenotypes induced in the specialized aphid predators were adaptive for development in aphid colonies, whereas that induced in the generalist was not. These results indicate that nonconsumptive effects are not simply a vertical force acting on prey, but can also impact conspecific and heterospecific competitors on the same trophic level.

Indigenous Aphid Predators Show High Levels of Preadaptation to a Novel Prey, Melanaphis sacchari (Hemiptera: Aphididae).

The performance of four aphid predators, Hippodamia convergens Guerin-Meneville, Coleomegilla maculata DeGeer, Chrysoperla carnea Stephens and Orius insidiosus Say was compared on three prey species: Schizaphis graminum Rondani, Melanaphis sacchari (Zehntner), and Ephestia kuehniella Zeller eggs. Species predatory in both life stages (all except Ch. carnea) were reared on E. kuehniella eggs and switched to aphid prey for assessment of reproduction. Differences were greater between the E. kuehniella and aphid diets than between the two aphid species. Juvenile survival was high for all predators on all prey, except for O. insidiosus, which had survival on E. kuehniella > S. graminum > M. sacchari. The fastest development of Ch. carnea and O. insidiosus was obtained on E. kuehniella, whereas H. convergens developed fastest on S. graminum, and C. maculata did not differ among diets. S. graminum also yielded the largest H. convergens adults, whereas the largest adults of other predators were obtained on E. kuehniella. Female fecundity and egg viability were similarly high on both aphid diets for H. convergens and C. maculata, whereas, on E. kuehniella, 50% of the former entered reproductive diapause and the latter species had reduced fecundity. Reproductive success of Ch. carnea was S. graminum = M. sacchari > E. kuehniella, but it was similar among treatments for O. insidiosus, although female infertility ranged from 25 to 37.5%. We concluded that all the predators studied are preadapted to utilize sugarcane aphid as prey and have excellent potential to provide sustainable biological control of this newly invasive pest.

Multiple Quantitative Trait Loci Influence the Shape of a Male-Specific Genital Structure in Drosophila melanogaster.

The observation that male genitalia diverge more rapidly than other morphological traits during evolution is taxonomically widespread and likely due to some form of sexual selection. One way to elucidate the evolutionary forces acting on these traits is to detail the genetic architecture of variation both within and between species, a program of research that is considerably more tractable in a model system. Drosophila melanogaster and its sibling species, D. simulans, D. mauritiana, and D. sechellia, are morphologically distinguishable only by the shape of the posterior lobe, a male-specific elaboration of the genital arch. We extend earlier studies identifying quantitative trait loci (QTL) responsible for lobe divergence across species and report the first genetic dissection of lobe shape variation within a species. Using an advanced intercross mapping design, we identify three autosomal QTL contributing to the difference in lobe shape between a pair of D. melanogaster inbred lines. The QTL each contribute 4.6-10.7% to shape variation, and two show a significant epistatic interaction. Interestingly, these intraspecific QTL map to the same locations as interspecific lobe QTL, implying some shared genetic control of the trait within and between species. As a first step toward a mechanistic understanding of natural lobe shape variation, we find an association between our QTL data and a set of genes that show sex-biased expression in the developing genital imaginal disc (the precursor of the adult genitalia). These genes are good candidates to harbor naturally segregating polymorphisms contributing to posterior lobe shape.