Simulation of early season herbivory via mechanical damage affects flower production in pumpkin (Cucurbita pepo ssp. pepo).

BACKGROUND: Damage from insect herbivores can elicit a wide range of plant responses, including reduced or compensatory growth, altered volatile profiles, or increased production of defence compounds. Specifically, herbivory can alter floral development as plants reallocate resources towards defence and regrowth functions. For pollinator-dependent species, floral quantity and quality are critical for attracting floral visitors; thus, herbivore-induced developmental effects that alter either floral abundance or attractiveness may have critical implications for plant reproductive success. Based on past work on resource trade-offs, we hypothesize that herbivore damage-induced effects are stronger in structural floral traits that require significant resource investment (e.g., flower quantity), as plants reallocate resources towards defence and regrowth, and weaker in secondary floral traits that require less structural investment (e.g., nectar rewards). SCOPE: In this study, we simulated early-season herbivore mechanical damage in the domesticated jack-o-lantern pumpkin Cucurbita pepo ssp. pepo and measured a diverse suite of floral traits over a 60-day greenhouse experiment. KEY RESULTS: We found that mechanical damage delayed the onset of male anthesis and reduced the total quantity of flowers produced. Additionally, permutational multivariate analysis of variance (PERMANOVA) indicated that mechanical damage significantly impacts overall floral volatile profile, though not output of sesquiterpenoids, a class of compounds known to recruit specialized cucumber beetle herbivores and squash bee pollinators. CONCLUSIONS: In summary, we show that C. pepo spp. pepo reduces investment in male flower production following mechanical damage, and that floral volatiles do exhibit shifts in production, indicative of damage-induced trait plasticity. Such reductions in male flower production could reduce the relative attractiveness of damaged plants to foraging pollinators in this globally relevant cultivated species.

Diet specialization mediates drivers of Cucurbita herbivory in a semi-arid agroecosystem.

Herbivory is a major fitness pressure for plants and a key driver of crop losses in agroecosystems. Dense monocultures are expected to favor specialist herbivorous insects, particularly those who primarily consume crop species; yet, levels and types of herbivory are not uniform within regional cropping systems. It is essential to determine which local and regional ecological factors drive variation in herbivory in order to support functional agroecosystems that rely less on chemical inputs. Crops in the genus Cucurbita host a suite of both generalist and specialist herbivores that inflict significant damage, yet little is known about the relative contribution of these herbivores to variation in herbivory and how local- and landscape-scale Cucurbita resource concentrations, management practices, and natural enemies mediate this relationship. In this study, we tested whether three foundational ecological hypotheses influenced Cucurbita herbivory across 20 pumpkin fields in the semi-arid Southern High Plains Region of Texas. We used generalized linear mixed models and confirmatory path analysis to assess whether the Density-dependent Herbivory Hypothesis, Resource Concentration Hypothesis, or the Natural Enemies Hypothesis, could explain variation in Cucurbita herbivory and insect dynamics in the context of conventional agronomic practices. We found that herbivory increased over time, indicating that herbivores were causing sustained damage throughout the growing season. We also found that fields with higher local Cucurbita resources had lower herbivory, suggesting a resource dilution effect. Natural enemy communities were more abundant and taxonomically rich in sites with greater generalist herbivore abundance, though predator abundance declined over time, indicating that late-season crop fields are most at risk given high herbivory and low natural enemy-based control. Our findings also suggest that while local resource availability may drive the abundance and richness of arthropod communities, additional agronomic and phenological information is needed to anticipate herbivory risk in an agriculturally dominated landscape.

A novel pesticide has lethal consequences for an important pollinator.

Wild bees pollinate crops and wildflowers where they are frequently exposed to pesticides. Neonicotinoids are the most commonly used insecticide globally, but restrictions on their use and rising pest resistance have increased the demand for alternative pesticides. Flupyradifurone is a novel insecticide that has been licenced globally for use on bee-visited crops. Here, in a semi-field experiment, we exposed solitary bees (Osmia lignaria) to a commercial pesticide formulation (Sivanto Prime) containing flupyradifurone at label-recommended rates. We originally designed the experiment to examine sublethal effects, but contrary to our expectations, 100 % of bees released into pesticide-treated cages died within 3 days of exposure, compared to 0 % in control plots. Bees exposed to flupyradifurone a few days after the initial application survived but endured prolonged sublethal effects, including lower nesting success, impairment to foraging efficiency, and higher mortality. These results demonstrate that exposure to this novel insecticide poses significant threats to solitary bees and add to a growing body of evidence indicating that this pesticide can have negative impacts on wild bees at field-realistic concentrations. In the short-term, we recommend that commercial formulations containing flupyradifurone should be restricted to non-flowering crops while a reassessment of its safety can be conducted. In the long-term, environmental risk assessors should continue to develop risk assessments that are truly holistic and incorporate the ecological and life history traits of multiple pollinator species.

Biogeography, climate, and land use create a mosaic of parasite risk in native bumble bees.

Host-parasite interactions are crucial to the regulation of host population growth, as they often impact both long-term population stability and ecological functioning. Animal hosts navigate a number of environmental conditions, including local climate, anthropogenic land use, and varying degrees of spatial isolation, all of which can mediate parasitism exposure. Despite this, we know little about the potential for these environmental conditions to impact pathogen prevalence at biogeographic scales, especially for key ecosystem service-providing animals. Bees are essential pollination providers that may be particularly sensitive to biogeography, climate, and land-use as these factors are known to limit bee dispersal and contribute to underlying population genetic variation, which may also impact host-parasite interactions. Importantly, many native bumble bee species have recently shown geographic range contractions, reduced genetic diversity, and increased parasitism rates, highlighting the potential importance of interacting and synergistic stressors. In this study, we incorporate spatially explicit environmental, biogeographic, and land-use data in combination with genetically derived host population data to conduct a large-scale epidemiological assessment of the drivers of pathogen prevalence across >1000 km for a keystone western US pollinator, the bumble bee Bombus vosnesenskii. We found high rates of infection from Crithidia bombi and C. expoekii, which show strong spatial autocorrelation and which were more prevalent in northern latitudes. We also show that land use barriers best explained differences in parasite prevalence and parasite community composition, while precipitation, elevation, and B. vosnesenskii nesting density were important drivers of parasite prevalence. Overall, our results demonstrate that human land use can impact critical host-parasite interactions for native bees at massive spatial scales. Further, our work indicates that disease-related survey and conservation measures should take into account the independent and interacting influences of climate, biogeography, land use, and local population dynamics.

Author Correction: A sulfotransferase dosage-dependently regulates mouthpart polyphenism in the nematode Pristionchus pacificus.

The original version of this Article contained errors in Figure 4. In panel a, the x axis labels of bars 6-11 were incorrect, as depicted in the associated Author Correction. These errors have been corrected in both the PDF and HTML versions of the Article.

A sulfotransferase dosage-dependently regulates mouthpart polyphenism in the nematode Pristionchus pacificus.

Polyphenism, the extreme form of developmental plasticity, is the ability of a genotype to produce discrete morphologies matched to alternative environments. Because polyphenism is likely to be under switch-like molecular control, a comparative genetic approach could reveal the molecular targets of plasticity evolution. Here we report that the lineage-specific sulfotransferase SEUD-1, which responds to environmental cues, dosage-dependently regulates polyphenism of mouthparts in the nematode Pristionchus pacificus. SEUD-1 is expressed in cells producing dimorphic morphologies, thereby integrating an intercellular signalling mechanism at its ultimate target. Additionally, multiple alterations of seud-1 support it as a potential target for plasticity evolution. First, a recent duplication of seud-1 in a sister species reveals a direct correlation between genomic dosage and polyphenism threshold. Second, inbreeding to produce divergent polyphenism thresholds resulted in changes in transcriptional dosage of seud-1. Our study thus offers a genetic explanation for how plastic responses evolve.

Specialization of a polyphenism switch gene following serial duplications in Pristionchus nematodes.

Polyphenism is an extreme manifestation of developmental plasticity, requiring distinct developmental programs and the addition of a switch mechanism. Because the genetic basis of polyphenism switches has only begun to be understood, how their mechanisms arise is unclear. In the nematode Pristionchus pacificus, which has a mouthpart polyphenism specialized for alternative diets, a gene (eud-1) executing the polyphenism switch was recently identified as the product of lineage-specific duplications. Here, we infer the role of gene duplications in producing a switch gene. Using reverse genetics and population genetic analyses, we examine evidence for competing scenarios of degeneration and complementation, neutral evolution, and functional specialization. Of the daughter genes, eud-1 alone has assumed switch-like regulation of the mouth polyphenism. Measurements of life-history traits in single, double, and triple sulfatase mutants did not, given a benign environment, identify alternative or complementary roles for eud-1 paralogs. Although possible roles are still unknown, selection analyses of the sister species and 104 natural isolates of P. pacificus detected purifying selection on the genes, suggesting their functionality by their fixation and evolutionary maintenance. Our approach shows the tractability of reverse genetics in a nontraditional model system to study evolution by gene duplication.

The Nuclear Hormone Receptor NHR-40 Acts Downstream of the Sulfatase EUD-1 as Part of a Developmental Plasticity Switch in Pristionchus.

Developmental plasticity, the ability of one genotype to produce distinct phenotypes in different environments, has been suggested to facilitate phenotypic diversification, and several examples in plants and animals support its macroevolutionary potential [1-8]. However, little is known about associated molecular mechanisms, because environmental effects on development are difficult to study by laboratory approaches. One promising system is the mouth dimorphism of the nematode Pristionchus pacificus [9-12]. Following an irreversible decision in larval development, these nematodes form moveable teeth that occur in either of two discrete morphs. The "eurystomatous" (Eu) form has a wide mouth and two teeth, allowing predatory feeding on other nematodes. In contrast, the alternative ("stenostomatous"; St) form has diminutive mouthparts that largely constrain its diet to microbes. The sulfatase EUD-1 was previously discovered to execute a polyphenism switch based on dosage of functional alleles [13] and confirmed a prediction of evolutionary theory about how developmental switches control plasticity [1, 3]. However, the genetic context of this single gene, and hence the molecular complexity of switch mechanisms, was previously unknown. Here we use a suppressor screen to identify factors downstream of eud-1 in mouth-form regulation. We isolated three dominant, X-linked mutants in the nuclear hormone receptor gene nhr-40 that are haploinsufficient. Both eud-1 nhr-40 double and nhr-40 single mutants are all Eu, whereas transgenic overexpression of nhr-40 does not restore the wild-type phenotype but instead results in nearly all-St lines. Thus, NHR-40 is part of a developmental switch, suggesting that switch mechanisms controlling plasticity consist of multi-component hormonal signaling systems.