Describing endosymbiont-host interactions within the parasitism-mutualism continuum.

Endosymbionts are widespread in arthropods, living in host cells with effects that extend from parasitic to mutualistic. Newly acquired endosymbionts tend to be parasitic, but vertical transmission favors coevolution toward mutualism, with hosts sometimes developing dependency. Endosymbionts negatively affecting host fitness may still spread by impacting host reproductive traits, referred to as reproductive "manipulation," although costs for hosts are often assumed rather than demonstrated. For cytoplasmic incompatibility (CI) that involves endosymbiont-mediated embryo death, theory predicts directional shifts away from "manipulation" toward reduced CI strength; moreover, CI-causing endosymbionts need to increase host fitness to initially spread. In nature, endosymbiont-host interactions and dynamics are complex, often depending on environmental conditions and evolutionary history. We advocate for capturing this complexity through appropriate datasets, rather than relying on terms like "manipulation." Such imprecision can lead to the misclassification of endosymbionts along the parasitism-mutualism continuum.

The effect of repeat feeding on dengue virus transmission potential in Wolbachia-infected Aedes aegypti following extended egg quiescence.

As Wolbachia pipientis is more widely being released into field populations of Aedes aegypti for disease control, the ability to select the appropriate strain for differing environments is increasingly important. A previous study revealed that longer-term quiescence in the egg phase reduced the fertility of mosquitoes, especially those harboring the wAlbB Wolbachia strain. This infertility was also associated with a greater biting rate. Here, we attempt to quantify the effect of this heightened biting behavior on the transmission potential of the dengue virus using a combination of assays for fitness, probing behavior, and vector competence, allowing repeat feeding, and incorporate these effects in a model of R0. We show that Wolbachia-infected infertile mosquitoes are more interested in feeding almost immediately after an initial blood meal relative to wild type and Wolbachia-infected fertile mosquitoes and that these differences continue for up to 8 days over the period we measured. As a result, the infertile Wolbachia mosquitoes have higher virus prevalence and loads than Wolbachia-fertile mosquitoes. We saw limited evidence of Wolbachia-mediated blocking in the disseminated tissue (legs) in terms of prevalence but did see reduced viral loads. Using a previously published estimate of the extrinsic incubation period, we demonstrate that the effect of repeat feeding/infertility is insufficient to overcome the effects of Wolbachia-mediated blocking on R0. These estimates are very conservative, however, and we posit that future studies should empirically measure EIP under a repeat feeding model. Our findings echo previous work where periods of extensive egg quiescence affected the reproductive success of Wolbachia-infected Ae. aegypti. Additionally, we show that increased biting behavior in association with this infertility in Wolbachia-infected mosquitoes may drive greater vector competence. These relationships require further exploration, given their ability to affect the success of field releases of Wolbachia for human disease reduction in drier climates where longer egg quiescence periods are expected.

Revisiting Wolbachia detections: Old and new issues in Aedes aegypti mosquitoes and other insects.

Wolbachia continue to be reported in species previously thought to lack them, particularly Aedes aegypti mosquitoes. The presence of Wolbachia in this arbovirus vector is considered important because releases of mosquitoes with transinfected Wolbachia are being used around the world to suppress pathogen transmission and these efforts depend on a lack of Wolbachia in natural populations of this species. We previously assessed papers reporting Wolbachia in natural populations of Ae. aegypti and found little evidence that seemed convincing. However, since our review, more and more papers are emerging on Wolbachia detections in this species. Our purpose here is to evaluate these papers within the context of criteria we previously established but also new criteria that include the absence of releases of transinfections within the local areas being sampled which has contaminated natural populations in at least one case where novel detections have been reported. We also address the broader issue of Wolbachia detection in other insects where similar issues may arise which can affect overall estimates of this endosymbiont more generally. We note continuing shortcomings in papers purporting to find natural Wolbachia in Ae. aegypti which are applicable to other insects as well.

Patterns and effects of gene flow on adaptation across spatial scales: implications for management.

Gene flow can have rapid effects on adaptation and is an important evolutionary tool available when undertaking biological conservation and restoration. This tool is underused partly because of the perceived risk of outbreeding depression and loss of mean fitness when different populations are crossed. In this article, we briefly review some theory and empirical findings on how genetic variation is distributed across species ranges, describe known patterns of gene flow in nature with respect to environmental gradients, and highlight the effects of gene flow on adaptation in small or stressed populations in challenging environments (e.g., at species range limits). We then present a case study involving crosses at varying spatial scales among mountain populations of a trigger plant (Stylidium armeria: Stylidiaceae) in the Australian Alps to highlight how some issues around gene flow effects can be evaluated. We found evidence of outbreeding depression in seed production at greater geographic distances. Nevertheless, we found no evidence of maladaptive gene flow effects in likelihood of germination, plant performance (size), and performance variance, suggesting that gene flow at all spatial scales produces offspring with high adaptive potential. This case study demonstrates a path to evaluating how increasing sources of gene flow in managed wild and restored populations could identify some offspring with high fitness that could bolster the ability of populations to adapt to future environmental changes. We suggest further ways in which managers and researchers can act to understand and consider adaptive gene flow in natural and conservation contexts under rapidly changing conditions.

Dengue Virus Serotype 1 Effects on Mosquito Survival Differ among Geographically Distinct Aedes aegypti Populations.

The mosquito Aedes aegypti is distributed worldwide and is recognized as the primary vector for dengue in numerous countries. To investigate whether the fitness cost of a single DENV-1 isolate varies among populations, we selected four Ae. aegypti populations from distinct localities: Australia (AUS), Brazil (BRA), Pakistan (PAK), and Peru (PER). Utilizing simple methodologies, we concurrently assessed survival rates and fecundity. Overall, DENV-1 infection led to a significant decrease in mosquito survival rates, with the exception of the PER population. Furthermore, infected Ae. aegypti from PAK, the population with the lowest infection rate among those tested, exhibited a noteworthy reduction in egg laying. These findings collectively suggest that local mosquito-virus adaptations may influence dengue transmission in endemic settings.

Wolbachia affect female mate preference and offspring fitness in a parasitoid wasp.

BACKGROUND: Wolbachia are widespread intracellular bacteria in insects that often have high rates of spread due to their impact on insect reproduction. These bacteria may also affect the mating behavior of their host with impacts on the fitness of host progeny. In this study, we investigated the impact of Wolbachia on a preference for mating with young or old males in the parasitoid wasp Habrobracon hebetor. RESULTS: Our results showed that uninfected females from a tetracycline-treated line preferred to mate with young males, whereas Wolbachia-infected females had no preference. Time to mating was relatively shorter in the infected lines. Regardless of Wolbachia infection status, progeny resulting from matings with young males showed higher fitness than those from crosses with old males, and infected females crossed with infected young males showed the highest performance. CONCLUSION: These results suggest an impact of Wolbachia on female mate preference and offspring fitness although it is unclear how this phenomenon increases Wolbachia transmission of infected wasps. © 2024 Society of Chemical Industry.

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.

Acute toxicity effects of pesticides on predatory snout mites (Trombidiformes: Bdellidae).

Predatory mites biologically control a range of arthropod crop pests and are often central to agricultural IPM strategies globally. Conflict between chemical and biological pest control has prompted increasing interest in selective pesticides with fewer off-target impacts on beneficial invertebrates, including predatory mites. However, the range of predatory mite species included in standardized pesticide toxicity assessments does not match the diversity of naturally occurring species contributing to biocontrol, with most testing carried out on species from the family Phytoseiidae (Mesostigmata). Here, we aim to bridge this knowledge gap by investigating the impacts of 22 agricultural pesticides on the predatory snout mite, Odontoscirus lapidaria (Kramer) (Trombidiformes: Bdellidae). Using internationally standardized testing methodologies, we identified several active ingredients with minimal impact on O. lapidaria mortality, including Bacillus thuringiensis, nuclear polyhedrosis virus, flonicamid, afidopyropen, chlorantraniliprole, and cyantraniliprole, which may therefore be good candidates for IPM strategies utilizing both chemical and biological control. Comparison of our findings with previous studies on Phytoseiid mites reveals important differences in responses to a number of chemicals between predatory mite families, including the miticides diafenthiuron and abamectin, highlighting the risk of making family-level generalizations from acute toxicity assessments. We also tested the impacts of several pesticides on a second Bdellidae species (Trombidiformes: Bdellidae) and found differences in the response to chlorpyrifos compared with O. lapidaria, further highlighting the taxon-specific nature of nontarget toxicity effects.

The monsoon-associated equine South African pointy mosquito 'Aedes caballus'; the first comprehensive record from southeastern Iran with a description of ecological, morphological, and molecular aspects.

The equine South African pointy vector mosquito, Aedes caballus, poses a significant threat to human health due to its capacity for transmitting arboviruses. Despite favorable climate for its existence in southeast Iran, previous records of this species in the area have indicated very low abundance. This comprehensive field and laboratory study aimed to assess its current adult population status in this region, utilizing a combination of ecological, morphological and molecular techniques. Four distinct types of traps were strategically placed in three fixed and two variable mosquito sampling sites in the southern strip of Sistan and Baluchistan Province. Subsequently, DNA was extracted from trapped mosquitoes and subjected to PCR amplification using the molecular markers COI, ITS2, and ANT. In total, 1734 adult Ae. caballus specimens were collected from rural areas, with the majority being captured by CO2-baited bednet traps. A notable increase in the abundance of this species was observed following rainfall in February. The genetic analysis revealed multiple haplotypes based on COI and ITS2 sequences, with COI gene divergence at 0.89%, and ITS2 sequence divergence at 1.6%. This suggests that previous challenges in morphological identification may have led to misidentifications, with many adults previously classified as Ae. vexans potentially being Ae. caballus. The findings of this study hold significant implications for public health authorities, providing valuable insights for integrated and targeted vector control and disease management efforts.

Wolbachia infection status and molecular diversity in the species of tribe Tagiadini Mabille, 1878 (Lepidoptera: Hesperiidae) collected in China.

Wolbachia, one of the most ubiquitous heritable symbionts in lepidopteran insects, can cause mitochondrial introgression in related host species. We recently found mito-nuclear discordance in the Lepidopteran tribe Tagiadini Mabille 1878 from which Wolbachia has not been reported. In this study, we found that 13 of the 46 species of Tagiadini species tested were positive for Wolbachia. Overall, 14% (15/110) of Tagiadini specimens were infected with Wolbachia and nine new STs were found from 15 isolates. A co-phylogenetic comparison, divergence time estimation and Wolbachia recombination analysis revealed that mito-nuclear discordance in Tagiadini species is not mediated by Wolbachia, but Wolbachia acquisition in Tagiadini appears to have occurred mainly through horizontal transmission rather than codivergence.

Acute toxicity effects of pesticides on beneficial organisms - Dispelling myths for a more sustainable use of chemicals in agricultural environments.

Agricultural practitioners, researchers and policymakers are increasingly advocating for integrated pest management (IPM) to reduce pesticide use while preserving crop productivity and profitability. Using selective pesticides, putatively designed to act on pests while minimising impacts on off-target organisms, is one such option - yet evidence of whether these chemicals control pests without adversely affecting natural enemies and other beneficial species (henceforth beneficials) remains scarce. At present, the selection of pesticides compatible with IPM often considers a single (or a limited number of) widely distributed beneficial species, without considering undesired effects on co-occurring beneficials. In this study, we conducted standardised laboratory bioassays to assess the acute toxicity effects of 20 chemicals on 15 beneficial species at multiple exposure timepoints, with the specific aims to: (1) identify common and diverging patterns in acute toxicity responses of tested beneficials; (2) determine if the effect of pesticides on beetles, wasps and mites is consistent across species within these groups; and (3) assess the impact of mortality assessment timepoints on International Organisation for Biological Control (IOBC) toxicity classifications. Our work demonstrates that in most cases, chemical toxicities cannot be generalised across a range of beneficial insects and mites providing biological control, a finding that was found even when comparing impacts among closely related species of beetles, wasps and mites. Additionally, we show that toxicity impacts increase with exposure length, pointing to limitations of IOBC protocols. This work challenges the notion that chemical toxicities can be adequately tested on a limited number of 'representative' species; instead, it highlights the need for careful consideration and testing on a range of regionally and seasonally relevant beneficial species.

Hormetic effect induced by Beauveria bassiana in Myzus persicae.

BACKGROUND: Myzus persicae, a serious sap-sucking pest of a large variety of host plants in agriculture, is traditionally controlled using chemical insecticides but there is interest in using biopesticides as restrictions are increasingly placed on the use of broad-spectrum pesticides. RESULTS: Here, we show that in Petri dish experiments, high concentrations of the fungal entomopathogen Beauveria bassiana led to rapid mortality of M. persicae, although at a low concentration (1 × 104 conidia mL-1) there is a hormetic effect in which survival and fecundity are enhanced. Hormetic effects persisted across a generation with reduced development time and increased fecundity in the offspring of M. persicae exposed to B. bassiana. The whole-plant experiment points to a hormetic effect being detected in two out of three tested lines. The impact of these effects might also depend on whether M. persicae was transinfected with the endosymbiont Rickettsiella viridis, which decreases fecundity and survival compared with aphids lacking this endosymbiont. This fecundity cost was ameliorated in the generation following exposure to the entomopathogen. CONCLUSION: Although B. bassiana is effective in controlling M. persicae especially at higher spore concentrations, utilization of this entomopathogen requires careful consideration of hormetic effects at lower spore concentrations, and further research to optimize its application for sustainable agriculture is recommended. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Wolbachia strains wMel and wAlbB differentially affect Aedes aegypti traits related to fecundity.

Two Wolbachia strains, wMel and wAlbB, have been transinfected into Aedes aegypti mosquitoes for population replacement with the aim of reducing dengue transmission. Epidemiological data from various endemic sites suggest a pronounced decrease in dengue transmission after implementing this strategy. In this study, we investigated the impact of the Wolbachia strains wMel and wAlbB on Ae. aegypti fitness in a common genetic background. We found that Ae. aegypti females infected with the wMel strain exhibited several significant differences compared with those infected with the wAlbB strain. Specifically, wMel-infected females laid significantly fewer eggs, ingested a lower amount of blood, had a reduced egg production rate, and exhibited a decreased Wolbachia density at a later age compared with mosquitoes infected with the wAlbB strain. Conversely, the wAlbB strain showed only mild negative effects when compared with Wolbachia-uninfected specimens. These differential effects on Ae. aegypti fitness following infection with either wMel or wAlbB may have important implications for the success of population replacement strategies in invading native Ae. aegypti populations in endemic settings. Further research is needed to better understand the underlying mechanisms responsible for these differences in fitness effects and their potential impact on the long-term efficacy of Wolbachia-based dengue control programs.IMPORTANCEThe transmission of arboviruses such as dengue, Zika, and chikungunya is on the rise globally. Among the most promising strategies to reduce arbovirus burden is the release of one out of two strains of Wolbachia-infected Aedes aegypti: wMel and wAlbB. One critical aspect of whether this approach will succeed involves the fitness cost of either Wolbachia strains on mosquito life history traits. For instance, we found that wMel-infected Ae. aegypti females laid significantly fewer eggs, ingested a lower amount of blood, had a reduced egg production rate, and exhibited a decreased Wolbachia density at a later age compared with mosquitoes infected with the wAlbB strain. Conversely, the wAlbB strain showed only mild negative effects when compared with Wolbachia-uninfected specimens. These differential effects on mosquito fitness following infection with either wMel or wAlbB may have important implications for the success of population replacement strategies in invading native Ae. aegypti populations.

Defence and nutrition synergistically contribute to the distinct tolerance of rice subspecies to the stem borer, Chilo suppressalis.

Damage caused by the rice striped stem borer (SSB), Chilo suppressalis (Walker) (Lepidoptera: Pyralidae), is much more severe on indica/xian rice than on japonica/geng rice (Oryza sativa) which matches pest outbreak data in cropping regions of China. The mechanistic basis of this difference among rice subspecies remains unclear. Using transcriptomic, metabolomic and genetic analyses in combination with insect bioassay experiments, we showed that japonica and indica rice utilise different defence responses to repel SSB, and that SSB exploited plant nutrition deficiencies in different ways in the subspecies. The more resistant japonica rice induced patterns of accumulation of methyl jasmonate (MeJA-part of a defensive pathway) and vitamin B1 (VB1-a nutrition pathway) distinct from indica cultivars. Using gene-edited rice plants and SSB bioassays, we found that MeJA and VB1 jointly affected the performance of SSB by disrupting juvenile hormone levels. In addition, genetic variants of key biosynthesis genes in the MeJA and VB1 pathways (OsJMT and OsTH1, respectively) differed between japonica and indica rice and contributed to performance differences; in indica rice, SSB avoided the MeJA defence pathway and hijacked the VB1 nutrition-related pathway to promote development. The findings highlight important genetic and mechanistic differences between rice subspecies affecting SSB damage which could be exploited in plant breeding for resistance.

Introduction of Aedes aegypti mosquitoes carrying wAlbB Wolbachia sharply decreases dengue incidence in disease hotspots.

Partial replacement of resident Aedes aegypti mosquitoes with introduced mosquitoes carrying certain strains of inherited Wolbachia symbionts can result in transmission blocking of dengue and other viruses of public health importance. Wolbachia strain wAlbB is an effective transmission blocker and stable at high temperatures, making it particularly suitable for hot tropical climates. Following trial field releases in Malaysia, releases using wAlbB Ae. aegypti have become operationalized by the Malaysian health authorities. We report here on an average reduction in dengue fever of 62.4% (confidence intervals 50-71%) in 20 releases sites when compared to 76 control sites in high-rise residential areas. Importantly the level of dengue reduction increased with Wolbachia frequency, with 75.8% reduction (61-87%) estimated at 100% Wolbachia frequency. These findings indicate large impacts of wAlbB Wolbachia invasions on dengue fever incidence in an operational setting, with incidence expected to further decrease as wider areas are invaded.

Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae).

There is growing interest in insecticide resistance in the mosquito, Aedes albopictus (Skuse), as its potential for spreading diseases is increasing as urbanization and control efforts intensify. Here we review the presence and diversity of mutations in the voltage-sensitive sodium channel (Vssc) gene associated with pyrethroid resistance and report on additional surveys of these mutations in new populations with an analysis of their spread. The known diversity of these mutations has increased in recent years including the identification of 26 non-synonymous mutations, although phenotypic data associating mutations with resistance remain limited. We provide data on mutations in several new locations including those in Timor Leste, Indonesia, and Vanuatu. We use population genomic data from ddRAD analyses of target populations with the 1534C mutation to identify single nucleotide polymorphisms (SNPs) associated with the mutant to test for clustering of SNPs based on the presence of the 1534C mutation rather than population origin. Our findings suggest spread of resistance alleles via genetic invasion, which is further supported by patterns from a genome-wide principal components analysis. These data point to movement of resistance alleles across wide areas with likely impacts on local control options.

Rapid and Repeated Climate Adaptation Involving Chromosome Inversions following Invasion of an Insect.

Following invasion, insects can become adapted to conditions experienced in their invasive range, but there are few studies on the speed of adaptation and its genomic basis. Here, we examine a small insect pest, Thrips palmi, following its contemporary range expansion across a sharp climate gradient from the subtropics to temperate areas. We first found a geographically associated population genetic structure and inferred a stepping-stone dispersal pattern in this pest from the open fields of southern China to greenhouse environments of northern regions, with limited gene flow after colonization. In common garden experiments, both the field and greenhouse groups exhibited clinal patterns in thermal tolerance as measured by critical thermal maximum (CTmax) closely linked with latitude and temperature variables. A selection experiment reinforced the evolutionary potential of CTmax with an estimated h2 of 6.8% for the trait. We identified 3 inversions in the genome that were closely associated with CTmax, accounting for 49.9%, 19.6%, and 8.6% of the variance in CTmax among populations. Other genomic variations in CTmax outside the inversion region were specific to certain populations but functionally conserved. These findings highlight rapid adaptation to CTmax in both open field and greenhouse populations and reiterate the importance of inversions behaving as large-effect alleles in climate adaptation.

Plasticity of cold and heat stress tolerance induced by hardening and acclimation in the melon thrips.

Extreme temperatures threaten species under climate change and can limit range expansions. Many species cope with changing environments through plastic changes. This study tested phenotypic changes in heat and cold tolerance under hardening and acclimation in the melon thrips, Thrips palmi Karny (Thysanoptera: Thripidae), an agricultural pest of many vegetables. We first measured the critical thermal maximum (CTmax) of the species by the knockdown time under static temperatures and found support for an injury accumulation model of heat stress. The inferred knockdown time at 39 °C was 82.22 min. Rapid heat hardening for 1 h at 35 °C slightly increased CTmax by 1.04 min but decreased it following exposure to 31 °C by 3.46 min and 39 °C by 6.78 min. Heat acclimation for 2 and 4 days significantly increased CTmax at 35 °C by 1.83, and 6.83 min, respectively. Rapid cold hardening at 0 °C and 4 °C for 2 h, and cold acclimation at 10 °C for 3 days also significantly increased cold tolerance by 6.09, 5.82, and 2.00 min, respectively, while cold hardening at 8 °C for 2 h and acclimation at 4 °C and 10 °C for 5 days did not change cold stress tolerance. Mortality at 4 °C for 3 and 5 days reached 24.07 % and 43.22 % respectively. Our study showed plasticity for heat and cold stress tolerance in T. palmi, but the thermal and temporal space for heat stress induction is narrower than for cold stress induction.

Mosquitoes provide a transmission route between possums and humans for Buruli ulcer in southeastern Australia.

Buruli ulcer, a chronic subcutaneous infection caused by Mycobacterium ulcerans, is increasing in prevalence in southeastern Australia. Possums are a local wildlife reservoir for M. ulcerans and, although mosquitoes have been implicated in transmission, it remains unclear how humans acquire infection. We conducted extensive field survey analyses of M. ulcerans prevalence among mosquitoes in the Mornington Peninsula region of southeastern Australia. PCR screening of trapped mosquitoes revealed a significant association between M. ulcerans and Aedes notoscriptus. Spatial scanning statistics revealed overlap between clusters of M. ulcerans-positive Ae. notoscriptus, M. ulcerans-positive possum excreta and Buruli ulcer cases, and metabarcoding analyses showed individual mosquitoes had fed on humans and possums. Bacterial genomic analysis confirmed shared single-nucleotide-polymorphism profiles for M. ulcerans detected in mosquitoes, possum excreta and humans. These findings indicate Ae. notoscriptus probably transmit M. ulcerans in southeastern Australia and highlight mosquito control as a Buruli ulcer prevention measure.