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.
The rapid pace of conversion of natural areas to agricultural systems is highly concerning, and the consequences for conservation and pest management are not yet fully understood. We examined mitochondrial (COI and Cytb) and nuclear (ITS1) gene regions of 21 populations of the stink bug Euschistus heros, to investigate the genetic diversity, genetic structure, and demographic history of this emerging soybean pest in South America. Two deep lineages that diverged in the Pliocene (4.5 Myr) occur over wide areas of Brazil. Historical changes during the Plio-Pleistocene led to significant genetic differences between E. heros populations, which differentiated further in several biomes. The northern lineage is older, more diverse, and prevalent in the Amazon and Caatinga, while the southern lineage is younger, less diverse, and prevalent in the Atlantic Forest and Chaco biomes. Euschistus heros populations are expanding in size and range but at different rates, strongly affected by environmental variables. Secondary contact between the main lineages is now occurring, mainly in areas of intensive farming and particularly in the Cerrado, an important agricultural frontier. Individuals adapted to different environmental conditions and to large monocultures might currently be combining into a panmictic and hard-to-control pest population.
BACKGROUND: Spodoptera frugiperda is a destructive pest that often imposes difficult management due to its high polyphagy and rapid insecticide resistance evolution. Knowledge of species diversification, population structure, and host preference can aid efforts to manage pest populations. Here, we investigated the patterns of hybridization, genetic structure, and gene flow in S. frugiperda populations, discussing how we can apply this knowledge to insect resistance management programs in South America. RESULTS:The corn-strain CS-h2 of S. frugiperda was the most frequent haplotype in all sampled populations. Spodoptera frugiperda populations are experiencing demographic expansion, and the ecoregions partially explain the genetic structure and not strains. We did not find a correlation between gene flow and susceptibility levels to flubendiamide and lufenuron insecticides, but populations with high LC 50 sent a great number of migrants to all other locations, maintaining resistance alleles in the geographic range. CONCLUSION: High levels of population admixture, including between corn-and rice-strains, were found in sampled populations. We showed that S. frugiperda immigrants will not necessarily cause an increase in LC 50 upon arrival in a new location but will assure the constant presence of resistance alleles in the area. Increases in LC 50 largely depend on the local pesticide management adopted in the areas. Our results indicate that pesticide resistance management must be adopted on a local or small regional scale.
Recent changes in soybean management like the adoption of transgenic crops and no-till farming, in addition to the expansion of cultivated areas into new virgin frontiers, are some of the hypotheses that can explain the rise of secondary pests, such as the Neotropical brown stink bug, Euschistus heros, in Brazil. To better access the risk of increased pests like E. heros and to determine probabilities for insecticide resistance spreading, it is necessary first to access the levels of the genetic diversity, how the genetic diversity is distributed, and how natural selection is acting upon the natural variation. Using the genotyping by sequencing (GBS) technique, we generated ~60,000 single-nucleotide polymorphisms (SNPs) distributed across the E. heros genome to answer some of those questions. The SNP data was used to investigate the pattern of genetic structure, hybridization and natural selection of this emerging pest. We found that E. heros populations presented similar levels of genetic diversity with slightly higher values at several central locations in Brazil. Our results also showed strong genetic structure separating northern and southern Brazilian regions (FST = 0.22; p-value = 0.000) with a very distinct hybrid zone at the central region. The analyses also suggest the possibility that GABA channels and odorant receptors might play a role in the process of natural selection. At least one marker was associated with soybean and beans crops, but no association between allele frequency and cotton was found. We discuss the implications of these findings in the management of emerging pests in agriculture, particularly in the context of large areas of monoculture such as soybean and cotton.
Background Invasion of organisms into new ecosystems is increasingly common, due to the global trade in commodities. One of the most complex post-invasion scenarios occurs when an invasive species is related to a native pest, and even more so when they can hybridize and produce fertile progeny. The global pest Helicoverpa armigera was first detected in Brazil in 2013 and generated a wave of speculations about the possibility of hybridization with the native sister taxon Helicoverpa zea. In the present study, we used genome-wide single nucleotide polymorphisms from field-collected individuals to estimate hybridization between H. armigera and H. zea in different Brazilian agricultural landscapes. Results The frequency of hybridization varied from 15 to 30% depending on the statistical analyses. These methods showed more congruence in estimating that hybrids contained approximately 10% mixed ancestry (i.e. introgression) from either species. Hybridization also varied considerably depending on the geographic locations where the sample was collected, forming a ‘mosaic’ hybrid zone where introgression may be facilitated by environmental and landscape variables. Both landscape composition and bioclimatic variables indicated that maize and soybean cropland are the main factors responsible for high levels of introgression in agricultural landscapes. The impact of multiple H. armigera incursions is reflected in the structured and inbred pattern of genetic diversity. Conclusions Our data showed that the landscape composition and bioclimatic variables influence the introgression rate between H. armigera and H. zea in agricultural areas. Continuous monitoring of the hybridization process in the field is necessary, since agricultural expansion, climatic fluctuations, changing composition of crop species and varieties, and dynamic planting seasons are some factors in South America that could cause a sudden alteration in the introgression rate between Helicoverpa species. Introgression between invasive and native pests can dramatically impact the evolution of host ranges and resistance management.
The sugarcane borer moth, Diatraea saccharalis , is one of the most important pests of sugarcane and maize crops in the Western Hemisphere. The pest is widespread throughout South and Central America, the Caribbean region and the southern United States. One of the most intriguing features of D . saccharalis population dynamics is the high rate of range expansion reported in recent years. To shed light on the history of colonization of D . saccharalis , we investigated the genetic structure and diversity in American populations using single nucleotide polymorphism (SNPs) markers throughout the genome and sequences of the mitochondrial gene cytochrome oxidase (COI). Our primary goal was to propose possible dispersal routes from the putative center of origin that can explain the spatial pattern of genetic diversity. Our findings showed a clear correspondence between genetic structure and the geographical distributions of this pest insect on the American continents. The clustering analyses indicated three distinct groups: one composed of Brazilian populations, a second group composed of populations from El Salvador, Mexico, Texas and Louisiana and a third group composed of the Florida population. The predicted time of divergence predates the agriculture expansion period, but the pattern of distribution of haplotype diversity suggests that human-mediated movement was most likely the factor responsible for the widespread distribution in the Americas. The study of the early history of D . saccharalis promotes a better understanding of range expansion, the history of invasion, and demographic patterns of pest populations in the Americas.
Unravelling the details of range expansion and ecological dominance shifts of insect pests has been challenging due to the lack of basic knowledge about population structure, gene flow, and most importantly, how natural selection is affecting the adaptive process. Piezodous guildinii is an emerging pest of soybean in the southern region of the United States, and increasingly important in Brazil in recent years. However, the reasons P. guildinii is gradually becoming more of a problem are questions still mostly unanswered. Here, we have genotyped P. guildinii samples and discovered 1,337 loci containing 4,083 variant sites SNPs that were used to estimate genetic structure and to identify gene candidates under natural selection. Our results revealed the existence of a significant genetic structure separating populations according to their broad geographic origin, i.e., U.S. and Brazil, supported by AMOVA (FGT = 0.26), STRUCTURE, PCA, and FST analyses. High levels of gene flow or coancestry within groups (i.e., within countries) can be inferred from the data, and no spatial pattern was apparent at the finer scale in Brazil. Samples from different seasons show more heterogeneous compositions suggesting mixed ancestry and a more complex dynamic. Lastly, we were able to detect and successfully annotated 123 GBS loci (10.5%) under positive selection. The gene ontology (GO) analysis implicated candidate genes under selection with genome reorganization, neuropeptides, and energy mobilization. We discuss how these findings could be related to recent outbreaks and suggest how new efforts directed to better understand P. guildinii population dynamics.
Population genetic structure of agricultural pests can be impacted not only by geographic distance and the broader ecological and physical barriers but also by patterns related to where crops are produced and how they are moved after harvest. Stored-product pests, for instance, specialize in exploiting grains such as wheat and rice from on-farm storage through transportation to final processing at often geographically distant locations; therefore human-aided movement may impact their dispersal. Although stored product insects are associated with stored grain, they can also exploit resources in the surrounding environments so different ecological regions where the grain is grown and stored may also influence population structure. Here we used 1,156 SNP markers to investigate how geographic distance, ecological and agricultural variables can impact the genetic structure and gene flow of the stored food pest beetle Rhyzopertha dominica . We found a substantial degree of admixture between weakly structured populations in the US. Ecological regions were more important in explaining R. dominica population structure than crop type, suggesting insect movement between wheat and rice grain distribution channels. We have also found a significant correlation between the genetic and geographical distance ( i.e. , isolation by distance). However, our modeling approach combining the ecological and management variables has highlighted the importance of the volume of grain received by a location in the dispersal dynamics of the pest. The first-generation migrant analysis offered additional supported to movement over great distances that are likely associated with grain movement. Our data suggest that a multitude of factors play small but significant parts in the movement dynamics of the pest. The beetles can take advantage of the source-sink dynamic of grain movement in the US, but also engage in a high rate of movement at the local scale. Understanding population structure for R. dominica will provide insights into the potential for local processes of adaptation and broader patterns of movement that will impact management programs and the potential for spread of resistance genes.
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