Transgenic crops producing Bacillus thuringiensis- (Bt) insecticidal proteins (Bt crops) have provided useful pest management tools to growers for the past 20 years. Planting Bt crops has reduced the use of synthetic insecticides on cotton, maize and soybean fields in 11 countries throughout Latin America. One of the threats that could jeopardize the sustainability of Bt crops is the development of resistance by targeted pests. Governments of many countries require vigilance in measuring changes in Bt-susceptibility in order to proactively implement corrective measures before Bt-resistance is widespread, thus prolonging the usefulness of Bt crops. A pragmatic approach to obtain information on the effectiveness of Bt-crops is directly asking growers, crop consultants and academics about Bt-resistance problems in agricultural fields, first-hand information that not necessarily relies on susceptibility screens performed in laboratories. This type of information is presented in this report. Problematic pests of cotton and soybeans in five Latin American countries currently are effectively controlled by Bt crops. Growers that plant conventional (non-Bt) cotton or soybeans have to spray synthetic insecticides against multiple pests that otherwise are controlled by these Bt crops. A similar situation has been observed in six Latin American countries where Bt maize is planted. No synthetic insecticide applications are used to control corn pests because they are controlled by Bt maize, with the exception of Spodoptera frugiperda. While this insect in some countries is still effectively controlled by Bt maize, in others resistance has evolved and necessitates supplemental insecticide applications and/or the use of Bt maize cultivars that express multiple Bt proteins. Partial control of S. frugiperda in certain countries is due to its natural tolerance to the Bt bacterium. Of the 31 pests targeted and controlled by Bt crops in Latin America, only S. frugiperda has shown tolerance to certain Bt proteins in growers' fields, the most reliable indication of the status of Bt-susceptibility in most of the American continent.

Current situation of pests targeted by Bt crops in Latin America

The fall armyworm (FAW) Spodoptera frugiperda (J. E. Smith) is a species native to the Americas. This polyphagous lepidopteran pest was first reported in Nigeria and the Democratic Republic of Sao Tome and Principe in 2016, but its presence in eastern Africa has not been confirmed via molecular characterisation. In this study, FAW specimens from western and central Uganda were identified based on the partial mtDNA COI gene sequences, with mtDNA COI haplotypes matching those identified in Nigeria and Sao Tome. In this study, we sequence an additional partial mtDNA Cyt b gene and also the partial mtDNA COIII gene in Ugandan FAW samples. We detected identical mitochondrial DNA haplotypes for both the mtDNA Cyt b and COI partial genes, while combining the mtDNA COI/Cyt b haplotypes and mtDNA COIII haplotypes enabled a new maternal lineage in the Ugandan corn-preferred FAW samples to be identified. Our results suggested that the African incursions of S. frugiperda involved at least three maternal lineages. Recent full genome, phylogenetic and microsatellite analyses provided evidence to support S. frugiperda as likely consisted of two sympatric sister species known as the corn-preferred and rice-preferred strains. In our Ugandan FAW populations, we identified the presence of mtDNA haplotypes representative of both sister species. It is not known if both FAW sister species were originally introduced together or separately, and whether they have since spread as a single population. Further analyses of additional specimens originally collected from Sao Tome, Nigeria and throughout Africa would be required to clarify this issue. Importantly, our finding showed that the genetic diversity of the African corn-preferred FAW species is higher than previously reported. This potentially contributed to the success of FAW establishment in Africa. Furthermore, with the additional maternal lineages detected, there is likely an increase in paternal lineages, thereby increasing the diversity of the African FAW population. Knowledge of the FAW genetic diversity will be needed to assess the risks of introducing Bt-resistance traits and to understand the FAW incursion pathways into the Old World and its potential onward spread. The agricultural implications of the presence of two evolutionary divergent FAW lineages (the corn and the rice lineage) in the African continent are further considered and discussed.

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Detection of sister-species in invasive populations of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) from Uganda.

Since its detection in Brazil in 2013, the Old World cotton bollworm Helicoverpa armigera has been reported in Argentina, Paraguay, and Bolivia. Here we present evidence extending the South American range of H. armigera to Uruguay, using polymerase chain reaction and sequencing of the partial mitochondrial DNA (mtDNA) cytochrome oxidase I region. Molecular characterization of this gene region from individuals from Paraguay also supports previous morphological identification of H. armigera in Paraguay. Shared mtDNA haplotypes in H. armigera from Brazil, Uruguay, and Paraguay were identified. Additional surveying of populations in this region will be imperative to better monitor and understand factors that are underpinning its presence and successful adaptation in these South American regions. We discuss our findings with respect to the development of resistance pest management strategies of this invasive insect pest in a predominantly monoculture soybean crop landscape in the Southern Cone region.

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Mitochondrial DNA COI characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) from Paraguay and Uruguay.

The Heliothinae complex in Argentina encompasses Helicoverpa gelotopoeon (Dyar), Helicoverpa zea (Boddie), Helicoverpa armigera (Hubner), and Chloridea virescens (Fabricius). In Tucuman, the native species H. gelotopoeon is one of the most voracious soybean pests and also affects cotton and chickpea, even more in soybean-chickpea succession cropping systems. Differentiation of the Heliothinae complex in the egg, larva, and pupa stages is difficult. Therefore, the observation of the adult wing pattern design and male genitalia is useful to differentiate species. The objective of this study was to identify the species of the Heliothinae complex, determine population fluctuations of the Heliothinae complex in soybean and chickpea crops using male moths collected in pheromone traps in Tucuman province, and update the geographical distribution of H. armigera in Argentina. The species found were H. gelotopoeon, H. armigera, H. zea, and C. virescens. Regardless of province, county, crop, and year, the predominant species was H. gelotopoeon Considering the population dynamics of H. gelotopoeon and H. armigera in chickpea and soybean crops, H. gelotopoeon was the most abundant species in both crops, in all years sampled, and the differences registered were significant. On the other hand, according to the Sistema Nacional Argentino de Vigilancia y Monitoreo de Plagas (SINAVIMO) database and our collections, H. armigera was recorded in eight provinces and 20 counties of Argentina, and its larvae were found on soybean, chickpea, sunflower crops and spiny plumeless thistle (Carduus acanthoides). This is the first report of H. armigera in sunflower and spiny plumeless thistle in Argentina.

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Species From the Heliothinae Complex (Lepidoptera: Noctuidae) in Tucumán, Argentina, an Update of Geographical Distribution of Helicoverpa armigera.

\n Since its introduction and establishment in Brazil in 2013 and subsequent spread through most of Latin America, the Old World bollworm, Helicoverpa armigera (Hübner), has become an economically important pest of soybean, cotton, and other crops. Because this pest can migrate long distances aided by wind currents, it is expected to arrive and establish in the United States. There were reports of H. armigera moth incursions collected in pheromone traps from Puerto Rico and Florida, but no reports yet of field establishment in the United States. Although H. armigera is a polyphagous pest and poses threats to multiple crops, it has shown preference for and is considered a key pest of soybean and cotton in Brazil. Soybean and cotton in Mid-Southern states will be at greater risk for economic loss when this pest establishes in the United States due to similarities of H. armigera with the native sibling species, Helicoverpa zea (Lepidoptera: Noctuidae) (Boddie). Both are polyphagous, could damage the same crops, and have documented cases of resistance. Establishment of H. armigera in the United States presents uncertainty about how the two species may interact in U.S. agroecosystems. Management strategies for H. armigera consist of correct species identification, monitoring and early detection, and determining the susceptibility of populations to multiple control tactics to deploy effective management tools. Although it is expected to be a key pest of soybean and cotton, in this article, we discuss the overview of the potential threats which H. armigera poses to soybean production in Mid-Southern states when it establishes in the United States.

Overview of Pest Status, Potential Risk, and Management Considerations of Helicoverpa armigera (Lepidoptera: Noctuidae) for U.S. Soybean Production

Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae: Heliothinae) is among the most voracious global pests of agriculture. Adults of this species were identified recently in northern Argentina by dissection of male genitalia. In this work, a rapid and simple molecular tool was designed to distinguish H. armigera from the morphologically similar indigenous bollworms Helicoverpa zea (Boddie) and Helicoverpa gelotopoeon (Dyar), regardless of the life stage. Amplification of partial COI gene with a new primer pair, and subsequent digestion with endonuclease HinfI, yielded different RFLP profiles for the three main Helicoverpa pests currently present in South America. The method was validated in Helicoverpa specimens collected across Argentina, whose identity was further corroborated by COI sequencing and phylogenetic analysis. The data reported here constitute the first molecular confirmation of this pest in the country. The survey revealed the occurrence of H. armigera in northern and central Argentina, including the main soybean- and maize-producing area.

https://bioone.org/journals/Journal-of-Economic-Entomology/volume-108/issue-6/tov254/Molecular-Identification-of-Helicoverpa-armigera-Lepidoptera--Noctuidae--Heliothinae/10.1093/jee/tov254.pdf

Molecular Identification of Helicoverpa armigera (Lepidoptera: Noctuidae: Heliothinae) in Argentina and Development of a Novel PCR-RFLP Method for its Rapid Differentiation From H. zea and H. gelotopoeon

The polyphagous Helicoverpa armigera (Lepidoptera: Noctuidae) causes significant agricultural losses worldwide. This pest has recently expanded its range into South America. Since its first report in north-western Argentina, H. armigera has already been detected in geographically distant locations within the country. In this work, mitochondrial cytochrome c oxidase subunit I (COI) and cytochrome b (Cytb) sequences obtained from H. armigera individuals collected in central and northern Argentina were analyzed to explore genetic variability. Five COI haplotypes and three Cytb haplotypes were detected among ten sequenced specimens (seven haplotypes if considering concatenated sequences). Thus, even with a limited number of samples, a high number of haplotypes was found, suggesting the occurrence of several female founder lineages of H. armigera in the country. With one exception, these mtDNA haplotypes were shared with H. armigera specimens from the neighboring countries of Brazil, Paraguay and/or Uruguay. However, the impact of natural migration and intercontinental agricultural trade on the establishment and spread of H. armigera in Argentina and other Latin-American countries is still a matter of research.

Evidence for multiple maternal lineages of the invasive pest Helicoverpa armigera in Argentina

Unveiling the occurrence of Melanaphis sorghi in Argentina following a major aphid outbreak

The Helicoverpa/Heliothis complex can cause serious damage to agricultural crops. Phenotypic similarity makes it difficult to discriminate between closely related Helicoverpa species. Currently, morphology of the male genitalia complemented with molecular techniques constitutes the best approach for species identification. In this work, a broad microscopic examination of adult Helicoverpa zea (Boddie) males (n = 200) captured in central Argentina was carried out in order to provide a detailed description of the valvae and the phallus. A considerable degree of variability was recorded. Both rounded and sharp valve apices were observed and valvae were not always parallel-sided. Most evident differences were detected concerning the number of cornuti on the phallus. A range of 15-21 cornuti per phallus was recorded, the mode being 18. A significant minority of the samples (3.5%) displayed an abnormal genital condition showing a constricted phallus lacking cornuti, and pointed valvae. This form was initially attributed to a distinct species, Heliothis stombleri, and later proposed as a synonym of H. zea based on additional morphological observations and molecular studies. Here, a phylogenetic analysis combining mitochondrial (cytochrome oxidase subunit I) and nuclear (elongation factor -1 alpha) genes was performed on these and other Helicoverpa specimens collected in the same geographical region, in order to further verify the taxonomic status of H. stombleri. The tree topology clearly grouped H. stombleri with H. zea, supporting the assumption that the former represents, in fact, an anomalous form of the latter. Further experiments are needed to clarify the etiology of this anomaly and its persistence over time.

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Further Description of Helicoverpa zea (Lepidoptera: Noctuidae) Male Genitalia and New Genetic Evidence of Synonymy With Respect to the Anomalous Form, “Heliothis stombleri”

Emilia Ines Balbi

Papers

Molecular Identification of Helicoverpa armigera (Lepidoptera: Noctuidae: Heliothinae) in Argentina and Development of a Novel PCR-RFLP Method for its Rapid Differentiation From H. zea and H. gelotopoeon

Evidence for multiple maternal lineages of the invasive pest Helicoverpa armigera in Argentina

Unveiling the occurrence of Melanaphis sorghi in Argentina following a major aphid outbreak

Further Description of Helicoverpa zea (Lepidoptera: Noctuidae) Male Genitalia and New Genetic Evidence of Synonymy With Respect to the Anomalous Form, “Heliothis stombleri”

First genetic analysis of Euschistus heros F. (Hemiptera: Pentatomidae) from Argentina and its relative abundance in a newly invaded soybean region