Novel transinfections of Rickettsiella do not affect insecticide tolerance in Myzus persicae, Rhopalosiphum padi, or Diuraphis noxia (Hemiptera: Aphididae).

Aphids (Hemiptera: Aphidoidea) are economically important crop pests worldwide. Because of growing issues with insecticide resistance and environmental contamination by insecticides, alternate methods are being explored to provide aphid control. Aphids contain endosymbiotic bacteria that affect host fitness and could be targeted as potential biocontrol agents, but such novel strategies should not impact the effectiveness of traditional chemical control. In this work, we used a novel endosymbiont transinfection to examine the impact of the endosymbiont Rickettsiella viridis on chemical tolerance in 3 important agricultural pest species of aphid: Myzus persicae (Sulzer) (Hemiptera: Aphididae), Rhopalosiphum padi (Linnaeus) (Hemiptera: Aphididae), and Diuraphis noxia (Mordvilko ex Kurdjumov) (Hemiptera: Aphididae). We tested tolerance to the commonly used insecticides alpha-cypermethrin, bifenthrin, and pirimicarb using a leaf-dip bioassay. We found no observed effect of this novel endosymbiont transinfection on chemical tolerance, suggesting that the strain of Rickettsiella tested here could be used as a biocontrol agent without affecting sensitivity to insecticides. This may allow Rickettsiella transinfections to be used in combination with chemical applications for pest control. The impacts of other endosymbionts on insecticide tolerance should be considered, along with tests on multiple aphid clones with different inherent levels of chemical tolerance.

Discovery of insecticide resistance in field-collected populations of the aphid pest, Acyrthosiphon kondoi Shinji.

BACKGROUND: The bluegreen aphid (Acyrthosiphon kondoi) is a worldwide pest of alfalfa, pulses, and other legume crops. An overreliance on insecticides to control A. kondoi has potentially placed populations under selection pressure favouring resistant phenotypes, but to date, there have been no documented cases of insecticide resistance. Recently, Australian growers began reporting that conventional insecticides were failing to adequately control A. kondoi populations, prompting this laboratory-based investigation into whether these populations have evolved resistance. RESULTS: We discovered four A. kondoi populations with moderate resistance (10-40-fold) to three different insecticide groups: organophosphates, carbamates and pyrethroids. However, A. kondoi populations showed no resistance to the butenolide, flupyradifurone. We were unable to identify general metabolic mechanisms using synergist assays (cytochromes P450, glutathione S-transferases, or esterases), indicating that further detailed molecular investigations to characterise the putative resistance mechanism are needed. CONCLUSION: Insecticide-resistant A. kondoi present an emerging challenge to Australian agriculture. Growers require new tools and updated strategies, including access to newer chemistries, to alleviate their reliance on the few insecticides currently registered against A. kondoi. The implications of insecticide resistant A. kondoi for future management, the potential mechanisms of resistance, and future research priorities are discussed. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

From laboratory to field: laboratory-measured pesticide resistance reflects outcomes of field-based control in the redlegged earth mite, Halotydeus destructor.

Resistance to pesticides is typically identified via laboratory bioassays after field control failures are observed, but the results of such assays are rarely validated through experiments under field conditions. Such validation is particularly important when only a low-to-moderate level of resistance is detected in the laboratory. Here we undertake such a validation for organophosphate resistance in the agricultural pest mite Halotydeus destructor, in which low-to-moderate levels of resistance to organophosphorus pesticides have evolved in Australia. Using data from laboratory bioassays, we show that resistance to the organophosphate chlorpyrifos is higher (around 100-fold) than resistance to another organophosphate, omethoate (around 7-fold). In field trials, both these chemicals were found to effectively control pesticide-susceptible populations of H. destructor. However, when applied to a resistant mite population in the field, the effectiveness of chlorpyrifos was substantially decreased. In contrast, omethoate remained effective when tested alone or as a mixture with chlorpyrifos. We also show that two novel (non-pesticide) treatments, molasses and wood vinegar, are ineffective in controlling H. destructor when sprayed to pasture fields at rates of 4 L/ha. These findings suggest a close link between levels of resistance quantified through laboratory bioassays and the field effectiveness of pesticides; however, in the case of H. destructor, this does not necessarily mean all field populations possessing organophosphate resistance will respond similarly given the potentially complex nature of the underlying resistance mechanism(s).

P450-mediated resistance in Myzus persicae (Sulzer) (Hemiptera: Aphididae) reduces the efficacy of neonicotinoid seed treatments in Brassica napus.

BACKGROUND: The prophylactic use of seeds treated with neonicotinoid insecticides remains an important means of controlling aphid pests in canola (Brassica napus) crops in many countries. Yet, one of the most economically important aphid species worldwide, the peach potato aphid (Myzus persicae), has evolved mechanisms which confer resistance to neonicotinoids, including amplification of the cytochrome P450 gene, CYP6CY3. While CYP6CY3 amplification has been associated with low-level resistance to several neonicotinoids in laboratory acute toxicity bioassays, its impact on insecticide efficacy in the field remains unresolved. In this study, we investigated the impact of CYP6CY3 amplification on the ability of M. persicae to survive neonicotinoid exposure under laboratory and semi-field conditions. RESULTS: Three M. persicae clones, possessing different copy numbers of CYP6CY3, were shown to respond differently when exposed to the neonicotinoids, imidacloprid and thiamethoxam, in laboratory bioassays. Two clones, EastNaernup209 and Osborne171, displayed low levels of resistance (3-20-fold), which is consistent with previous studies. However, in a large-scale semi-field trial, both clones showed a surprising ability to survive and reproduce on B. napus seedlings grown from commercial rates of neonicotinoid-treated seed. In contrast, an insecticide-susceptible clone, of wild-type CYP6CY3 copy number, was unable to survive on seedlings treated in the same manner. CONCLUSION: Our findings suggest that amplification of CYP6CY3 in M. persicae clones substantially impairs the efficacy of neonicotinoid seed treatments when applied to B. napus. These findings highlight the potentially important real-world implications of resistances typically considered to be 'low level' as defined through laboratory bioassays. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Barley Yellow Dwarf Virus Influences Its Vector's Endosymbionts but Not Its Thermotolerance.

The barley yellow dwarf virus (BYDV) of cereals is thought to substantially increase the high-temperature tolerance of its aphid vector, Rhopalosiphum padi, which may enhance its transmission efficiency. This is based on experiments with North American strains of BYDV and R. padi. Here, we independently test these by measuring the temperature tolerance, via Critical Thermal Maximum (CTmax) and knockdown time, of Australian R. padi infected with a local BYDV isolate. We further consider the interaction between BYDV transmission, the primary endosymbiont of R. padi (Buchnera aphidicola), and a transinfected secondary endosymbiont (Rickettsiella viridis) which reduces the thermotolerance of other aphid species. We failed to find an increase in tolerance to high temperatures in BYDV-infected aphids or an impact of Rickettsiella on thermotolerance. However, BYDV interacted with R. padi endosymbionts in unexpected ways, suppressing the density of Buchnera and Rickettsiella. BYDV density was also fourfold higher in Rickettsiella-infected aphids. Our findings indicate that BYDV does not necessarily increase the temperature tolerance of the aphid transmission vector to increase its transmission potential, at least for the genotype combinations tested here. The interactions between BYDV and Rickettsiella suggest new ways in which aphid endosymbionts may influence how BYDV spreads, which needs further testing in a field context.

Spirotetramat resistance in Myzus persicae (Sulzer) (Hemiptera: Aphididae) and its association with the presence of the A2666V mutation.

BACKGROUND: Chemicals are widely used to protect field crops against aphid pests and aphid-borne viral diseases. One such species is Myzus persicae (Sulzer), a global pest that attacks a broad array of agricultural crops and transmits many economically damaging plant viruses. This species has evolved resistance to a large number of insecticide compounds as a result of widespread and repeated chemical use in many parts of the world. In this study, we investigated the evolution of resistance to a new plant protection product, spirotetramat, following reported chemical control failures. RESULTS: Our study provides clear phenotypic and genotypic evidence of spirotetramat resistance in populations of M. persicae from Australia. We show there is cross-resistance to other insecticides within the same chemical group, namely spiromesifen and spirodiclofen. We also demonstrate that resistance is associated with the previously reported mutation, A2226V in the target site of spirotetramat, acetyl-CoA carboxylase. Our genetic analysis found all resistant M. persicae populations belong to the same multi-locus clonal type and carry the A2226V mutation, which appears to be inherited as a dominant trait in this species. CONCLUSION: Our findings provide new insight into the resistance conferred by A2226V and have implications for the control of M. persicae in Australia and worldwide. A diagnostic assay developed in this study should serve as a valuable tool for future resistance monitoring and to support the implementation of pest management strategies. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Fungicides have transgenerational effects on Rhopalosiphum padi but not their endosymbionts.

BACKGROUND: While several agricultural fungicides are known to directly affect invertebrate pests, including aphids, the mechanisms involved are often unknown. One hypothesis is that fungicides with antibacterial activity suppress bacterial endosymbionts present in aphids which are important for aphid survival. Endosymbiont-related effects are expected to be transgenerational, given that these bacteria are maternally inherited. Here, we test for these associations using three fungicides (chlorothalonil, pyraclostrobin and trifloxystrobin) against the bird cherry-oat aphid, Rhopalosiphum padi, using a microinjected strain that carried both the primary endosymbiont Buchnera and the secondary endosymbiont Rickettsiella. RESULTS: We show that the fungicide chlorothalonil did not cause an immediate effect on aphid survival, whereas both strobilurin fungicides (pyraclostrobin and trifloxystrobin) decreased survival after 48 h exposure. However, chlorothalonil substantially reduced the lifespan and fecundity of the F1 generation. Trifloxystrobin also reduced the lifespan and fecundity of F1 offspring, however, pyraclostrobin did not affect these traits. None of the fungicides consistently altered the density of Buchnera or Rickettsiella in whole aphids. CONCLUSIONS: Our results suggest fungicides have sublethal impacts on R. padi that are not fully realized until the generation after exposure, and these sublethal impacts are not associated with the density of endosymbionts harbored by R. padi. However, we cannot rule out other effects of fungicides on endosymbionts that might influence fitness, like changes in their tissue distribution. We discuss these results within the context of fungicidal effects on aphid suppression across generations and point to potential field applications. © 2022 Society of Chemical Industry.

The thermal environment at fertilization mediates adaptive potential in the sea.

Additive genetic variation for fitness at vulnerable life stages governs the adaptive potential of populations facing stressful conditions under climate change, and can depend on current conditions as well as those experienced by past stages or generations. For sexual populations, fertilization is the key stage that links one generation to the next, yet the effects of fertilization environment on the adaptive potential at the vulnerable stages that then unfold during development are rarely considered, despite climatic stress posing risks for gamete function and fertility in many taxa and external fertilizers especially. Here, we develop a simple fitness landscape model exploring the effects of environmental stress at fertilization and development on the adaptive potential in early life. We then test our model with a quantitative genetic breeding design exposing family groups of a marine external fertilizer, the tubeworm Galeolaria caespitosa, to a factorial manipulation of current and projected temperatures at fertilization and development. We find that adaptive potential in early life is substantially reduced, to the point of being no longer detectable, by genotype-specific carryover effects of fertilization under projected warming. We interpret these results in light of our fitness landscape model, and argue that the thermal environment at fertilization deserves more attention than it currently receives when forecasting the adaptive potential of populations confronting climate change.

How does parental environment influence the potential for adaptation to global change?

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown. Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures. Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming. Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change?

Mounting research considers whether populations may adapt to global change based on additive genetic variance in fitness. Yet selection acts on phenotypes, not additive genetic variance alone, meaning that persistence and evolutionary potential in the near term, at least, may be influenced by other sources of fitness variation, including nonadditive genetic and maternal environmental effects. The fitness consequences of these effects, and their environmental sensitivity, are largely unknown. Here, applying a quantitative genetic breeding design to an ecologically important marine tubeworm, we examined nonadditive genetic and maternal environmental effects on fitness (larval survival) across three thermal environments. We found that these effects are nontrivial and environment dependent, explaining at least 44% of all parentally derived effects on survival at any temperature and 96% of parental effects at the most stressful temperature. Unlike maternal environmental effects, which manifested at the latter temperature only, nonadditive genetic effects were consistently significant and covaried positively across temperatures (i.e., parental combinations that enhanced survival at one temperature also enhanced survival at elevated temperatures). Thus, while nonadditive genetic and maternal environmental effects have long been neglected because their evolutionary consequences are complex, unpredictable, or seen as transient, we argue that they warrant further attention in a rapidly warming world.

Revealing hidden evolutionary capacity to cope with global change.

The extent to which global change will impact the long-term persistence of species depends on their evolutionary potential to adapt to future conditions. While the number of studies that estimate the standing levels of adaptive genetic variation in populations under predicted global change scenarios is growing all the time, few studies have considered multiple environments simultaneously and even fewer have considered evolutionary potential in multivariate context. Because conditions will not be constant, adaptation to climate change is fundamentally a multivariate process so viewing genetic variances and covariances over multivariate space will always be more informative than relying on bivariate genetic correlations between traits. A multivariate approach to understanding the evolutionary capacity to cope with global change is necessary to avoid misestimating adaptive genetic variation in the dimensions in which selection will act. We assessed the evolutionary capacity of the larval stage of the marine polychaete Galeolaria caespitosa to adapt to warmer water temperatures. Galeolaria is an important habitat-forming species in Australia, and its earlier life-history stages tend to be more susceptible to stress. We used a powerful quantitative genetics design that assessed the impacts of three temperatures on subsequent survival across over 30 000 embryos across 204 unique families. We found adaptive genetic variation in the two cooler temperatures in our study, but none in the warmest temperature. Based on these results, we would have concluded that this species has very little capacity to evolve to the warmest temperature. However, when we explored genetic variation in multivariate space, we found evidence that larval survival has the potential to evolve even in the warmest temperatures via correlated responses to selection across thermal environments. Future studies should take a multivariate approach to estimating evolutionary capacity to cope with global change lest they misestimate a species' true adaptive potential.