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    The mitogenome of Halotydeus destructor (Tucker) and its relationships with other trombidiform mites as inferred from nucleotide sequences and gene arrangements
    Thia, JA ; Young, ND ; Korhnen, PK ; Yang, Q ; Gasser, RB ; Umina, PA ; Hoffmann, AA (WILEY, 2021-10)
    The redlegged earth mite, Halotydeus destructor (Tucker, 1925: Trombidiformes, Eupodoidea, Penthaleidae), is an invasive mite species. In Australia, this mite has become a pest of winter pastures and grain crops. We report the complete mitogenome for H. destructor, the first to represent the family Penthaleidae, superfamily Eupodoidea. The mitogenome of H. destructor is 14,691 bp in size, and has a GC content of 27.87%, 13 protein-coding genes, two rRNA genes, and 22 tRNA genes. We explored evolutionary relationships of H. destructor with other members of the Trombidiformes using phylogenetic analyses of nucleotide sequences and the order of protein-coding and rRNA genes. We found strong, consistent support for the superfamily Tydeoidea being the sister taxon to the superfamily Eupodoidea based on nucleotide sequences and gene arrangements. Moreover, the gene arrangements of Eupodoidea and Tydeoidea are not only identical to each other but also identical to that of the hypothesized arthropod ancestor, showing a high level of conservatism in the mitogenomic structure of these mite superfamilies. Our study illustrates the utility of gene arrangements for providing complementary information to nucleotide sequences with respect to inferring the evolutionary relationships of species within the order Trombidiformes. The mitogenome of H. destructor provides a valuable resource for further population genetic studies of this important agricultural pest. Given the co-occurrence of closely related, morphologically similar Penthaleidae mites with H. destructor in the field, a complete mitogenome provides new opportunities to develop metabarcoding tools to study mite diversity in agro-ecosystems. Moreover, the H. destructor mitogenome fills an important taxonomic gap that will facilitate further study of trombidiform mite evolution.
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    High Incidence of Related Wolbachia across Unrelated Leaf-Mining Diptera
    Xu, X ; Ridland, PM ; Umina, PA ; Gill, A ; Ross, PA ; Pirtle, E ; Hoffmann, AA (MDPI, 2021-09)
    The maternally inherited endosymbiont, Wolbachia pipientis, plays an important role in the ecology and evolution of many of its hosts by affecting host reproduction and fitness. Here, we investigated 13 dipteran leaf-mining species to characterize Wolbachia infections and the potential for this endosymbiont in biocontrol. Wolbachia infections were present in 12 species, including 10 species where the Wolbachia infection was at or near fixation. A comparison of Wolbachia relatedness based on the wsp/MLST gene set showed that unrelated leaf-mining species often shared similar Wolbachia, suggesting common horizontal transfer. We established a colony of Liriomyza brassicae and found adult Wolbachia density was stable; although Wolbachia density differed between the sexes, with females having a 20-fold higher density than males. Wolbachia density increased during L. brassicae development, with higher densities in pupae than larvae. We removed Wolbachia using tetracycline and performed reciprocal crosses between Wolbachia-infected and uninfected individuals. Cured females crossed with infected males failed to produce offspring, indicating that Wolbachia induced complete cytoplasmic incompatibility in L. brassicae. The results highlight the potential of Wolbachia to suppress Liriomyza pests based on approaches such as the incompatible insect technique, where infected males are released into populations lacking Wolbachia or with a different incompatible infection.
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    Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae.
    Singh, KS ; Cordeiro, EMG ; Troczka, BJ ; Pym, A ; Mackisack, J ; Mathers, TC ; Duarte, A ; Legeai, F ; Robin, S ; Bielza, P ; Burrack, HJ ; Charaabi, K ; Denholm, I ; Figueroa, CC ; Ffrench-Constant, RH ; Jander, G ; Margaritopoulos, JT ; Mazzoni, E ; Nauen, R ; Ramírez, CC ; Ren, G ; Stepanyan, I ; Umina, PA ; Voronova, NV ; Vontas, J ; Williamson, MS ; Wilson, ACC ; Xi-Wu, G ; Youn, Y-N ; Zimmer, CT ; Simon, J-C ; Hayward, A ; Bass, C (Springer Science and Business Media LLC, 2021-07-07)
    The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host-plant associations, uncovering the widespread co-option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.
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    Origin of resistance to pyrethroids in the redlegged earth mite (Halotydeus destructor) in Australia: repeated local evolution and migration
    Yang, Q ; Umina, PA ; Rasic, G ; Bell, N ; Fang, J ; Lord, A ; Hoffmann, AA (JOHN WILEY & SONS LTD, 2020-02)
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    Regional and seasonal activity predictions for fall armyworm in Australia.
    Maino, JL ; Schouten, R ; Overton, K ; Day, R ; Ekesi, S ; Bett, B ; Barton, M ; Gregg, PC ; Umina, PA ; Reynolds, OL (Elsevier BV, 2021)
    Since 2016, the fall armyworm (FAW), Spodoptera frugiperda, has undergone a significant range expansion from its native range in the Americas, to continental Africa, Asia, and in February 2020, mainland Australia. The large dispersal potential of FAW adults, wide host range of immature feeding stages, and unique environmental conditions in its invasive range creates large uncertainties in the expected impact on Australian plant production industries. Here, using a spatial model of population growth and spread potential informed by existing biological and climatic data, we simulate seasonal population activity potential of FAW, with a focus on Australia's grain production regions. Our results show that, in Australia, the large spread potential of FAW will allow it to exploit temporarily favourable conditions for population growth across highly variable climatic conditions. It is estimated that FAW populations would be present in a wide range of grain growing regions at certain times of year, but importantly, the expected seasonal activity will vary markedly between regions and years depending on climatic conditions. The window of activity for FAW will be longer for growing regions further north, with some regions possessing conditions conducive to year-round population survival. Seasonal migrations from this permanent range into southern regions, where large areas of annual grain crops are grown annually, are predicted to commence from October, i.e. spring, with populations subsequently building up into summer. The early stage of the FAW incursion into Australia means our predictions of seasonal activity potential will need to be refined as more Australian-specific information is accumulated. This study has contributed to our early understanding of FAW movement and population dynamics in Australia. Importantly, the models established here provide a useful framework that will be available to other countries should FAW invade in the future. To increase the robustness of our model, field sampling to identify conditions under which population growth occurs, and the location of source populations for migration events is required. This will enable accurate forecasting and early warning to farmers, which should improve pest monitoring and control programs of FAW.
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    Predicting the global invasion of Drosophila suzukii to improve Australian biosecurity preparedness
    Maino, JL ; Schouten, R ; Umina, P ; Elderd, B (WILEY, 2021-04)
    Predicting biological invasions remains a challenge to applied ecologists and limits pre‐emptive management of biosecurity threats. In the last decade, spotted‐wing drosophila Drosophila suzukii has emerged as an internationally significant agricultural pest as it rapidly spread across Europe and the Americas. However, the underlying drivers of its global invasion remain unstudied, while countries like Australia, presently free from D. suzukii, require robust estimates of spread and establishment potential to aid development of effective preparedness strategies. Here, we analysed the ecoclimatic and human‐mediated drivers of the global invasion of D. suzukii to understand historical spread patterns and improve forecasts of future spread potential. Using a modular approach, climate‐driven population dynamics were linked in space via dispersal processes to simulate spread at continental scales. Combined with biological parameters measured in laboratory studies, the spread model was parameterized and validated on international spread data. Model accuracy was high and was able to predict 83% of regional presence–absence through time in the United States and, without further model fitting, 78% of the variation in the Europe incursion. Omitting human‐assisted spread from the model reduced predictability by over 20%, highlighting the large anthropogenic influence in this modern biological invasion. Economic activity (GDP) rather than human population density was more strongly associated with human‐mediated spread. Simulations predicted that eastern Australian coastal regions, particularly those near major cities with high economic activity, will result in the fastest spread of D. suzukii. Synthesis and applications. Incursions of Drosophila suzukii into Australia will have significant consequences for horticultural industries with the predicted speed of spread making eradication programs extremely difficult. However, the identified areas of significant fruit production, and high environmental suitability and economic activity will form a logical means for prioritizing industry preparedness. In light of our findings, a key component of preparedness strategies will be the ability of fruit producers to rapidly transition to effective management of D. suzukii.
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    Empowering Australian insecticide resistance research with genetic information: the road ahead
    Thia, JA ; Hoffmann, AA ; Umina, PA (WILEY, 2021-02)
    Abstract Insecticides are important for chemical control of arthropod pests in agricultural systems but select for resistance as an adaptive trait. Identifying the genetic mechanism(s) underpinning resistance can facilitate development of genetic markers, which can be used in monitoring programs. Moreover, understanding of genetic mechanisms in a broader population genetic context can be used to infer the origins of resistance, predict the dynamics of resistance evolution and evaluate the efficacy of different management strategies. Transitioning genetic information successfully into practical solutions requires overcoming two major hurdles. Firstly, genetic mechanisms must be identified to develop genetic markers. Secondly, routine use of genetic markers is required to build substantial spatio‐temporal data on the distribution and frequency of resistance alleles. In this study, we demonstrate large knowledge gaps on the genetic mechanisms of insecticide resistances in Australia using eight established arthropod pests important to the grains industry: Bemisia tabaci (silverleaf whitefly), Frankliniella occidentalis (western flower thrips), Halotydeus destructor (redlegged earth mite), Helicoverpa armigera (cotton bollworm), Myzus persicae (green peach aphid), Plutella xylostella (diamondback moth), Tetranychus urticae (two‐spotted spider mite) and Thrips tabaci (onion thrips). Many resistances have not been characterised at the genetic level in most pests, even for chemical MoA groups with a long history of use in Australia. Moreover, monitoring of resistance is spatio‐temporally patchy, which precludes examination of long‐term trends or predictive modelling. We suggest that leveraging cumulative global knowledge of resistances to develop a priori candidate genes, and incorporation of genomic approaches, can help overcome the hurdles of embracing genetic information in resistance management. We highlight the recently invasive Spodoptera frugiperda (fall armyworm) as a case study where genetic markers and genomic approaches should prove useful in rapidly assessing the risk of this species to the Australian grains industry and other agricultural commodities. The uptake of genetic information into management can only occur once its benefit to empower insecticide resistance research is fully realised. Ultimately, the road ahead requires amalgamation of multifaceted data (genes, environment and spatio‐temporal replication) to better understand and predict the dynamics of resistance evolution.
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    Susceptibility of the bird cherry-oat aphid, Rhopalosiphum padi (Hemiptera: Aphididae), to four insecticides
    Umina, PA ; Reidy-Crofts, J ; Babineau, M ; Maino, JL ; Edwards, OR (WILEY, 2020-11)
    Abstract The bird‐cherry oat aphid (Rhopalosiphum padi) is a global pest, attacking most cereal crops including barley, wheat, oats and triticale. The aphids cause yield losses through direct feeding damage and the transmission of plant viruses. In Australia, feeding injury can reduce cereal yields by 6%, with the damage caused by aphid‐vectored viruses reducing the yield of cereal crops by up to 30%. Aphid control in these crops is achieved almost exclusively with insecticides, and there is growing concern surrounding insecticide resistance evolution in multiple aphid species. In this study, nine field populations of R. padi were collected from localities representing the major grain growing regions of Australia. Toxicity data against four insecticides (dimethoate, alpha‐cypermethrin, pirimicarb and imidacloprid) was generated for each aphid population. This revealed little differences in population responses for three of these insecticides. For alpha‐cypermethrin, a widely used insecticide in Australia, there were significant differences between several populations. These data will be important for future monitoring of insecticide responses of R. padi and highlight the impending pest management challenges growers could encounter in Australia.
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    Ontogeny in the European earwig (Forficula auricularia) and grain crops interact to exacerbate feeding damage risk
    Kirkland, LS ; Maino, J ; Stuart, O ; Umina, PA (Wiley, 2020-08-01)
    The preference of herbivores for different host plants can be modulated by plant ontogeny. In agricultural pest management, this has implications for sowing dates and pest monitoring. In the last 20 years, the European earwig (Forficula auricularia), a cosmopolitan pest, has been increasingly implicated in damage to grain crops in Australia. Among these, rapeseed, Brassica napus, appears especially at risk, but little information on F. auricularia as a grain pest is available. We tested the susceptibility of seven grain crops commonly grown in Australia to infestation by F. auricularia using closed microcosm experiments, exposing plant seedlings at two early growth stages to four different life stages of F. auricularia. Lucerne and rapeseed were shown to be the most vulnerable crops, and younger seedlings experienced significantly more damage than older seedlings across all crop types. Fourth instar F. auricularia were found to cause greater feeding damage than younger or older earwigs, while adults collected in winter generally caused more damage than those collected in summer. Surprisingly, even second instar F. auricularia caused greater damage than summer adults. This variation could reflect the ontogenetically dynamic nutritional needs of earwigs. Recent studies of F. auricularia's life cycle in southern Australia indicate that these damaging life stages have some overlap with sowing dates of the crops tested here, exposing their vulnerable seedling stage to infestation. The phenology of F. auricularia in southern Australia therefore partly drives its ability to act as a pest. Future monitoring will likely need to track the distribution of F. auricularia life stages in order to effectively mitigate risks to vulnerable crops.
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    Biology, ecology and management of Diuraphis noxia (Hemiptera: Aphididae) in Australia
    Ward, S ; van Helden, M ; Heddle, T ; Ridland, PM ; Pirtle, E ; Umina, PA (WILEY, 2020-05)
    Abstract The Russian wheat aphid, Diuraphis noxia (Mordvilko ex Kurdjumov), is one of the world's most economically important pests of grain crops and has been recorded from at least 140 grass species within Poaceae. It has rapidly dispersed from its native origin of Central Asia into most major grain‐producing regions of the world including Africa, Asia, Europe, the Middle East, North America and South America. Diuraphis noxia was first found in Australia in a wheat crop in the mid‐north of South Australia in May 2016. Since then, D. noxia has been recorded throughout grain‐growing regions of South Australia, Victoria, New South Wales and Tasmania. The distribution will continue to expand, with climatic suitability modelling suggesting D. noxia can persist in all key grain regions, including large parts of Western Australia and Queensland. Australian populations of D. noxia appear to be anholocyclic, with no sexual stages being observed. The aphids can reproduce year round as long as host plants are available. Australian farmers have generally adopted prophylactic insecticide seed treatments and/or foliar sprays to manage D. noxia. Research is required to fully understand yield impacts, host preferences and host plant resistance associated with D. noxia. Cultural control through managing alternate host plants over summer, agronomic crop management, biological control and developments in host plant resistance should provide considerable future benefits.