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Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys
Abstract and Figures
Identifying the origin of a biological invasion has important applications to the effective control of the invaders. This is more critical for invasive agricultural pests that cause severe economic losses. The brown marmorated stink bug, Halyomorpha halys, originally from East Asia, has become a principal agricultural pest in the US since its first detection in Pennsylvania in 1996. This species is responsible for crop failures on many mid-Atlantic farms and current control efforts rely on heavy insecticide applications because no other options are available. To examine the genetic diversity and identify the source region of the US introductions, we sequenced portions of the mitochondrial cytochrome c oxidase subunit II gene, 12S ribosomal RNA gene and control region in populations from the US, China, South Korea and Japan. We detected high genetic divergence among native populations and traced the origin of US H. halys to the Beijing area in China. We observed much lower genetic diversity in exotic compared to native populations—two mitochondrial haplotypes in 55 US specimens versus 43 haplotypes in 77 native specimens. A single introduction of small propagule size matches the invasion history in the US. For the effective control of the US population, we suggest that surveys on egg parasitoids and insecticide resistance in natives should focus on the Beijing area in China.
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January 2014
... We used the populations module of StackS version 2.58 (Rochette et al., 2019) to calculate overall nucleotide diversity (π), average observed and expected heterozygosity (H O and H E ), and average inbreeding coefficient F (F IS ; Wright, 1949) for each population. We used the r package StAMPP version 1.6.3 ...
... We used the r package StAMPP version 1.6.3 (Pembleton et al., 2013) to calculate population pairwise fixation indices (F ST ), according to the method proposed by Wright (1949) and updated by Weir and Cockerham (1984), using 100 bootstraps. We evaluated patterns of linkage disequilibrium (LD) decay across SNPs in each population with PopLDdecay version 3.42 (Zhang et al., 2019), using default parameters except changing the maximum distance between two SNPs setting to 1 kb to account for the lack of dense SNPs along short genomic scaffolds in our data set. ...
... Previous population genetic analyses using mitochondrial markers reported high haplotype diversity and spatial differentiation across BMSB's native range (Cesari et al., 2015;Valentin et al., 2017;Xu et al., 2014;. Genome-wide SNP data in our study confirmed these findings, showing China and Japan as two highly divergent clusters. ...
Abstract Invasive species are increasingly threatening ecosystems and agriculture by rapidly expanding their range and adapting to environmental and human‐imposed selective pressures. The genomic mechanisms that underlie such rapid changes remain unclear, especially for agriculturally important pests. Here, we use genome‐wide polymorphisms derived from native, invasive, and intercepted samples and populations of the brown marmorated stink bug (BMSB), Halyomorpha halys, to gain insights into population genomics processes that have promoted the successful global invasion of this polyphagous pest. Our analysis demonstrated that BMSB exhibits spatial structure but admixture rates are high among introduced populations, resulting in similar levels of genomic diversity across native and introduced populations. These spatial genomic patterns suggest a complex invasion scenario, potentially with multiple bridgehead events, posing a challenge for accurately assigning BMSB incursions to their source using reduced‐representation genomic data. By associating allele frequencies with the invasion status of BMSB populations, we found significantly differentiated SNPs located in close proximity to genes for insecticide resistance and olfaction. Comparing variations in allele frequencies among populations for outlier SNPs suggests that BMSB invasion success has likely evolved from standing genetic variation. In addition to being a major nuisance of households, BMSB has caused significant economic losses to agriculture in recent years and continues to expand its range. Despite no record of BMSB insecticide resistance to date, our results show high capacity for potential evolution of such characters, highlighting the need for future sustainable and targeted management strategies.
... Source tracing (also referred to as source estimation or identification; or origin tracing, determination, or inference; and as invasion history in the context of nonnative species) is an important tool for pest management in agro-ecosystems (Roderick 1996(Roderick , 2004. Molecular and genetic methods are widely used for source tracing across taxa, with many examples in insects (Izzo et al. 2018;Lesieur et al. 2019;Rugman-Jones et al. 2007;Xu et al. 2014). Source tracing of boll weevils aims to identify geographic sources of outbreaks in the USA and Mexico (Kim et al. , 2008. ...
... R/adegenet v2.1.5 was used to carry out the principal components analysis, estimate K using the K-means clustering algorithm, and carry out the discriminant analysis of principal components (Jombart 2008;Jombart and Ahmed 2011). The optimal K was selected by calculating and plotting the Bayesian Information Criterion (BIC) scores from the K-means analysis with R/ggplot2 v3.3.6 and choosing the value of K at which an asymptote was reached (Wickham 2016). ...
Anthonomus grandis Boheman (Coleoptera: Curculionidae) is comprised of two subspecies: the boll weevil (A. g. grandis) and the thurberia weevil (A. g. thurberiae). The thurberia weevil is generally regarded as a non-pest variant of the species, whereas the boll weevil is an important economic pest of commercial cotton. In the USA, a nationwide eradication program has been largely successful against the boll weevil, but reintroductions of eradicated zones remain a threat. In 2015, A. grandis was trapped in the functionally eradicated Winter Garden growing region in Texas, where it had not been found since 2012. Weevils established in the area and triggered a multi-year, multi-million-dollar mitigation effort. In 2017, the species was trapped in Hidalgo County, New Mexico, another area where it had been previously eradicated. In this study, we obtained specimens from both trapping events and used double digest restriction site-associated DNA sequencing to obtain genetic data in homology with previously published A. grandis population genetic data. We conducted source tracing to match the captured weevils to previously described populations to determine a likely source population. We also compared the accuracy of the approach to other diagnostic methods currently used by the United States Department of Agriculture. The results suggested that a small founder population of weevils dispersed from the Lower Rio Grande Valley population in southern Texas and northern Tamaulipas and established in the Winter Garden. In Hidalgo Co., NM, the weevils were found to be genetically indistinct from non-pest populations of thurberia weevil associated with Arizona wild cotton (Gossypium thurberi). Thurberia weevils in Arizona remain unlikely to threaten commercial growers. Improved rapid diagnostic tools may be desirable to enable better assessment of trap captures and allow for a reduction in the application of mitigation efforts when the non-pest variant is identified.
... It was also discovered in the USA and Switzerland, so it has potentially become a worldwide pest. The invasion of other regions by BMSB began in the mid-1990s in the USA when H. halys was recorded in Pennsylvania, and after few years, it spread to 40 states of the USA (Hoebeke and Carter 2003;Funayama 2012;Xu et al. 2014). It is an extremely polyphagous invasive pest, and it has spread all over the Northern Hemisphere rapidly since its first detection in the USA in 1990s and in Europe since 2004. ...
Your article is protected by copyright and all rights are held exclusively by Deutsche Phytomedizinische Gesellschaft. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com". Abstract The brown marmorated stink bug, Halyomorpha halys (Stål), is a pest of many annual and perennial agricultural products. The species is native to Asia. It is an awful highly polyphagous invasive pest. This study is the first comprehensive study on Halyomorpha halys (Stål) (Heteroptera: Pentatomidae), which is an invasive species in Turkey, and was conducted to determine the spread, intensity, population change and hosts of it in the Black Sea Region in 2018. In the present study, pheromone traps were placed for the pest in 6 cities, 49 counties and 149 locations between May and October, and were followed periodically. According to the results, it was determined that H. halys spread between Kemalpaşa (Artvin) and Hayrat (Trabzon). According to the number of the adults that were caught by the pheromone traps, the areas where the pest was at the highest intensity were: Hopa, Kemalpaşa, Borçka, Arhavi (Artvin) and Fındıklı (Rize). It was determined in the area where the study was conducted that many cultivated plants especially hazelnut, kiwi, corn, orange, blueberry, beans and tomato were the hosts of the pest, and recommendations were given on the precautions that must be taken against the pest.
... PCR priming sites are, therefore, at best, only conserved enough for very closely related species. Consequently, the effort and resources to develop the method by species have been constrained to those pests considered very high-risk based on their economic, environmental, or social impact and global invasion patterns [9][10][11][12][13][14]. Unfortunately, a lot of exotic insects which arrive, and those which may become established, do not have this status but represent potential hazards nonetheless, for which populationlevel data would be beneficial [15]. ...
Biosecurity responses to post-border exotic pest detections are more effective with knowledge of where the species may have originated from or if recurrent detections are connected. Population genetic markers for this are typically species-specific and not available in advance for any but the highest risk species, leaving other less anticipated species difficult to assess at the time. Here, new degenerate PCR primer sets are designed for within the Lepidoptera and Diptera for the 3′ COI, ND3, ND6, and 3′ plus 5′ 16S gene regions. These are shown to be universal at the ordinal level amongst species of 14 and 15 families across 10 and 11 dipteran and lepidopteran superfamilies, respectively. Sequencing the ND3 amplicons as an example of all the loci confirmed detection of population-level variation. This supported finding multiple population haplotypes from the publicly available sequences. Concatenation of the sequences also confirmed that higher population resolution is achieved than for the individual genes. Although as-yet untested in a biosecurity situation, this method is a relatively simple, off-the-shelf means to characterise populations. This makes a proactive contribution to the toolbox of quarantine agencies at the time of detection without the need for unprepared species-specific research and development.
... Populations subsequently spread and became established in most eastern and midwestern states and in at least four western states (StopBMSB.org). Low genetic diversity among H. halys in the eastern USA suggests these populations are the result of a single introduction from near Beijing, China, into eastern Pennsylvania (Xu et al. 2014;Valentin et al. 2017). Greater genetic diversity among western US populations suggest separate and multiple introductions from China (Valentin et al. 2017). ...
Brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive pest of Asian origin first detected in North Carolina in 2009. By 2015, it became an important pest in the mountain and Piedmont regions, but its population densities have remained low in the eastern plains regions. Starting with a cohort of diapausing adults in January of 2018 and 2019, semi-field cage studies were used to document the phenology and reproductive capacity of H. halys through October of each year at Mills River (mountains) and Goldsboro (Southeastern Plains) sites, which have the same photoperiod, but different temperature profiles. Halyomorpha halys was univoltine in the cooler mountain site, but bivoltine in the warmer plains site, leading to earlier emergence from overwintering diapause, greater heat unit accumulations, and a F1 adult generation that emerged before on-set of diapause-inducing conditions, which allowed for an F2 generation. However, only 17.2% of ovipositing F1 females laid egg masses that hatched, compared to > 90% of overwintered females. Poor establishment of H. halys in the plains versus mountains was attributed to heat stress that contributed to a higher percentage of overwintered adults that emerged early and did not oviposit, a truncated oviposition pattern by overwintered adults, and poor F2 egg hatch. Quadratic equations fit relationships between cumulative degree-days from biofix and proportional oviposition and adult eclosion of respective generations. Utility of the phenology model on a wider scale will depend on how well H. halys populations in other areas conform to North Carolina population’s response to photoperiod and temperature.
... The mitochondrial Cytochrome Oxidase I (COI) gene has shown utility in species identification and separation of genetic lineages (Bucklin et al. 2011;Stephens et al. 2011), in particular as it relates to reconstructing routes of invasion (Auger-Rozenberg et al. 2012;Chapman et al. 2015). Although the Cytochrome Oxidase II (COII) gene of H. halys has also been sequenced (Xu et al. 2014;Cesari et al. 2015Cesari et al. , 2018Yan et al. 2021), the COI gene has been used more extensively in the characterisation of the invasion history, diversity and identity of H. halys haplotypes in both native and invaded regions Cesari et al. 2015Cesari et al. , 2018Zhu et al. 2016;Morrison et al. 2017;Valentin et al. 2017;Lee et al. 2018;Horwood et al. 2019;Schuler et al. 2020;Yan et al. 2021). Based on the COI haplotype analysis of H. halys, it has been suggested that multiple invasion events took place in the initial / early stages of invasion in Europe (2007)(2008)(2009)(2010)(2011)(2012), with the population in Switzerland (primarily haplotype H3 and H8) resulting from the establishment of individuals that arrived directly from China; the population in Italy (primarily H1) resulting from the establishment of individuals from the invasive population in the USA; and the population in Greece (predominantly haplotype H33) resulting from a separate establishment of H. halys from China (Cesari et al. 2015;Gariepy et al. 2015;Valentin et al. 2017). ...
The arrival, establishment and pest status of Halyomorpha halys in Europe and non-native countries in Asia have been well-documented, with thorough characterisation of the genetic diversity and occurrence of cytochrome oxidase I (COI) haplotypes in Switzerland, France, Hungary, Italy and Greece. However, a number of gaps exist in terms of the characterisation of the haplotype diversity and occurrence of H. halys along the invasion front that covers eastern Europe, western and central Asia. To contribute towards filling this gap, the COI haplotype diversity and distribution were investigated for H. halys collected in Serbia, Ukraine, Russia, Georgia and Kazakhstan. A total of 646 specimens were analysed and five haplotypes were found (H1, H3, H8, H33 and H80). Haplotype H1 was present in all five countries investigated and was the only haplotype detected amongst > 500 specimens collected from Ukraine, Russia and Georgia. H1 (82%) was the dominant haplotype found in Kazakhstan, alongside H3 (18%). In contrast to the low or no diversity observed in these four countries, Serbia had higher haplotype diversity and was represented by five haplotypes. Although H3 was dominant (47%) in Serbia, H1 was also prevalent (40%); the remaining haplotypes (H8, H33 and H80) were minor contributors (1–11%) to the haplotype composition. The results are discussed in context with other known populations in neighbouring countries and patterns of haplotype diversity indicate the movement of successful invasive populations in Europe to generate secondary invasions along the eastern front of the invasion in Eurasia. Possible scenarios regarding the spread of particular haplotypes in these regions are discussed, along with suggestions for future research to fill existing gaps.
Threatening the global community is a wide variety of potential threats, most notably invasive pest species. Invasive pest species are non-native organisms that humans have either accidentally or intentionally spread to new regions. One of the most effective and first lines of control strategies for controlling pests is the application of insecticides. These toxic chemicals are employed to get rid of pests, but they pose great risks to people, animals, and plants. Pesticides are heavily used in managing invasive pests in the current era. Due to the overuse of synthetic chemicals, numerous invasive species have already developed resistance. The resistance development is the main reason for the failure to manage the invasive species. Developing pesticide resistance management techniques necessitates a thorough understanding of the mechanisms through which insects acquire insecticide resistance. Insects use a variety of behavioral, biochemical, physiological, genetic, and metabolic methods to deal with toxic chemicals, which can lead to resistance through continuous overexpression of detoxifying enzymes. An overabundance of enzymes causes metabolic resistance, detoxifying pesticides and rendering them ineffective against pests. A key factor in the development of metabolic resistance is the amplification of certain metabolic enzymes, specifically esterases, Glutathione S-transferase, Cytochromes p450 monooxygenase, and hydrolyses. Additionally, insect guts offer unique habitats for microbial colonization, and gut bacteria may serve their hosts a variety of useful services. Most importantly, the detoxification of insecticides leads to resistance development. The complete knowledge of invasive pest species and their mechanisms of resistance development could be very helpful in coping with the challenges and effectively developing effective strategies for the control of invasive species. Integrated Pest Management is particularly effective at lowering the risk of chemical and environmental contaminants and the resulting health issues, and it may also offer the most effective ways to control insect pests.
The brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive pest introduced to North America in the mid-1990's that has caused economic losses to a wide range of commodities. In vegetables, H. halys feeding damage has been well described, but the effect of different vegetable hosts on H. halys fitness is less understood. We caged 2nd instar H. halys on different vegetable hosts (e.g., tomato, sweet corn, eggplant, bell pepper, and snap bean) and monitored their development until adulthood to compare the effects of vegetable host type on H. halys nymph survival and development time. Experiments were replicated nine times over a two-year period. Survival of 2nd instars from F1 generation (early-season) eggs was low (<30%) on all vegetables resulting in no significant treatment effect. However, H. halys nymphs collected from F2 generation (late-season) eggs had higher survivorship on all vegetables except tomato. The percentage of H. halys 2nd instars that reached adulthood was greatest on corn (53%) and pepper (45%), followed by snap bean (24%), and significantly lower on eggplant (9%) and tomato (2%). Total development time from 2nd instar to adult was fastest on corn and slowest on peppers, although tomatoes were not tested due to the low survival. Trends in development rate were not seasonally-dependent. Our study compares H. halys survivability on several vegetable commodities, and provides insights into H. halys developmental success and dependence on various host plants over the season.
We monitored the seasonal abundance of Halyomorpha halys (Hemiptera: Pentatomidae) in forested areas near international ports and agricultural landscapes in South Korea from April to November in 2020 and 2021. Furthermore, flight capacity and reproductive status of field-collected H. halys adults during autumn dispersal period were evaluated. A total of 2,395 adults and 259 nymphs were collected, and population dynamics of adults showed similar patterns in forested areas near the ports and agricultural landscapes. Mean and maximum flight distances of adults collected from October to November, 2021, were 229 ± 71 m and 2,802 m, respectively, and all adults were nonreproductive except one male.
Brown marmorated stink bug (BMSB), native to East Asia, is an important agricultural and residential pest of having serious global concern. Since its first arrival to Pennsylvania in 1996, it has been dispersed in different states of USA and continuing to invade more. Not only in North America, this insect has invaded Europe, Australia, South America, recently to Africa and newer regions of Asia. These insects are reported to be highly efficient in terms of biological characteristics. Furthermore, due to absence of effective natural enemies in the newly invaded area, these insect's population is building extensively and causing severe damages to various crops. In the newly invaded areas, control options for these pests are limited till now and growers are mostly dependent on broad spectrum insecticides, which is not only costlier but also have negative consequences to the environment and biodiversity at large. Globalized trade has brought the risk of potential spread of this insect species to South Asian region from the native areas and newly invaded regions. The regions of having subtropical climate in South Asia may favor brown marmortaed stink bug's growth, development and population buildup and could bear losses to proliferating growers of vegetable and fruit crops. Therefore, it is crucial to monitor the movement and spread of this insect species to South Asia by following strong quarantine measures.
Episodes of population growth and decline leave characteristic signatures in the distribution of nucleotide (or restriction) site differences between pairs of individuals. These signatures appear in histograms showing the relative frequencies of pairs of individuals who differ by i sites, where i = 0, 1, .... In this distribution an episode of growth generates a wave that travels to the right, traversing 1 unit of the horizontal axis in each 1/2u generations, where u is the mutation rate. The smaller the initial population, the steeper will be the leading face of the wave. The larger the increase in population size, the smaller will be the distribution's vertical intercept. The implications of continued exponential growth are indistinguishable from those of a sudden burst of population growth Bottlenecks in population size also generate waves similar to those produced by a sudden expansion, but with elevated uppertail probabilities. Reductions in population size initially generate L-shaped distributions with high probability of identity, but these converge rapidly to a new equilibrium. In equilibrium populations the theoretical curves are free of waves. However, computer simulations of such populations generate empirical distributions with many peaks and little resemblance to the theory. On the other hand, agreement is better in the transient (nonequilibrium) case, where simulated empirical distributions typically exhibit waves very similar to those predicted by theory. Thus, waves in empirical distributions may be rich in information about the history of population dynamics.
Many animals and plants establish symbiotic associations with benevolent microorganisms. In particular, most of insects that feed exclusively on restricted diets, such as plant sap, vertebrate blood or woody material, usually possess symbiotic microorganisms inside their body. Recent studies have suggested that more than 50% of insect species may be benefited from such endosymbiotic partners. Among these insects, members of the Heteroptera, known as true bugs or stinkbugs, exhibit an extraordinary diversity in their microbial symbiotic system. Such diversity is exemplified by: (i) physiological impact of the symbiotic associations on the host fitness ranging from parasitic to mutualistic; (ii) interdependence of the symbiotic associations ranging from facultative to obligate; (iii) location of the symbiont ranging from extracellular in gut cavity to intracellular in specialized cells; (iv) among the extracellular associations, specialized symbiotic structures such as midgut sacs and tubular outgrowths, whose cavity harbors specific symbiotic bacteria, varying in their number and arrangement; and (v) mechanisms for symbiont transmission ranging from vertical to environmental. Here, the current biological knowledge of the diverse stinkbug-bacteria symbioses is reviewed, which will provide novel insights into and useful model systems for understanding of the host-symbiont interactions and evolution.
Over the past three decades there has been a dramatic increase in theoretical and practical studies on insect natural enemies. The appeal of insect predators, and parasitoids in particular, as research animals derives from the relative ease with which many species may be cultured and experimented with in the laboratory, the simple life cycles of most parasitoids, and the increasing demand for biological pest control. This considerably updated and expanded version of a previous best-seller is an account of major aspects of the biology of predators and parasitoids, punctuated with information and advice on which experiments or observations to conduct and how to carry them out. This book is unique in the field, as a general text emphasizing practicalities and providing guidance on further literature. It is ideal for students and professionals working in universities and both government and commercial institutes in the fields of pest management, agriculture, horticulture and forestry.