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Biology subjects

North, H. L.

Publications and source records attributed to North, H. L..

6 recordsLinked to original sources

Genetically informed distribution models refine predictions for the overwintering range of Helicoverpa armigera in North America

The ecological and economic threat posed by invasive pests demands proactive mitigation. Species distribution models (SDMs) are widely used in efforts to predict where invasive species might spread after introduction, though such models face several limitations. Among these is the unrealistic assumption of niche uniformity throughout a species' range. This has led to interest in developing SDMs that explicitly account for local adaptation, though few methods have achieved this in a way that confidently separates local adaptation from population structure. Here we develop and implement a sequential SDM approach that incorporates experimentally verified associations between genotype, phenotype, and environment to forecast establishment risk in a major agricultural pest. We leverage genomic data from 738 individuals to characterize the geographic distribution of alleles at a major-effect locus for cold tolerance (tret1) in Helicoverpa armigera, an invasive crop pest of major economic concern in North America. We demonstrate that a recently detected North American population carries a cold-adapted tret1 allele, which has likely contributed to its persistence. We quantify the contribution of cold-adapted tret1 to the potential invasive range of H. armigera in North America under current and future climate scenarios. We find that cold-adapted tret1 may dramatically expand the potential range of H. armigera, and that potential future range expansion is likely to be driven primarily by cold-adapted individuals. Our results highlight the importance of accounting for intraspecific variation in invasive species risk assessments and management strategies.

ecology↗

The collision of two genomes threatens global food security

Human activity alters selection pressures and redistributes biodiversity, creating opportunities for hybridization when dilerent species come into secondary contact. It is now well-established that ancient hybridization plays an important role in adaptive radiation 1, but its role in recent anthropogenic adaptation remains unclear. We investigated this in a study of hybridizing native and invasive Helicoverpa moths in Brazil, which are among the most economically damaging crop pests globally. Native H. zea has recently evolved Bt resistance and is better adapted to maize as a host plant, while invasive H. armigera is resistant to pyrethroid pesticides and is better adapted to soybean. Using a decade-long time series of 975 genomes from both species, we demonstrate rapid, bidirectional adaptive introgression of structural variants that cause resistance to two distinct pesticides. In one direction, a pyrethroid resistance gene from H. armigera (CYP337B3) is now almost fixed in native H. zea. In the other direction, ~30% of recently-sampled invasive H. armigera carry a H. zea-derived trypsin repeat cluster. Using controlled crosses, we show that this trypsin repeat cluster confers resistance to Bt (Cry1Ac) soy in the H. armigera genomic background. Thus, hybridization has combined H. armigera adaptation to soy with H. zea Cry1Ac resistance to facilitate exploitation of Brazilian Bt soy monoculture -- a vast anthropogenic habitat exceeding the area of Germany. Our results show that the combinatorial mechanisms that produce biodiversity can also drive rapid anthropogenic adaptation on ecological timescales, with consequences for global food security.

evolutionary biology↗

The genetic architecture of resistance to flubendiamide insecticides in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

Insecticide resistance is a major problem in food production, environmental sustainability, and human health. The cotton bollworm Helicoverpa armigera is a globally distributed crop pest affecting over 300 crop species. H. armigera has rapidly evolved insecticide resistance, making it one of the most damaging pests worldwide. Understanding the genetic basis of insecticide resistance provides insights to develop tools, such as molecular markers, that can be used to slow or prevent the evolution of resistance. We explore the genetic architecture of H. armigera resistance to a widely used insecticide, flubendiamide, using two complementary approaches: genome-wide association studies (GWAS) in wild-caught samples and quantitative trait locus (QTL) mapping in a controlled cross of susceptible and resistant laboratory strains. Both approaches identified one locus on chromosome 2, revealing two SNPs within 976 bp that can be used to monitor field resistance to flubendiamide. This was the only region identified using linkage mapping, though GWAS revealed additional sites associated with resistance. Other loci identified by GWAS in field populations contained known insecticide detoxification genes from the ATP-binding cassette family, ABCA1, ABCA3, ABCF2 and MDR1. Our findings revealed an oligogenic genetic architecture, in contrast to previous reports of monogenic resistance associated with the ryanodine receptor. This work elucidates the genetic basis of rapidly evolving insecticide resistance and will contribute to the development of effective insecticide resistance management strategies. Author summaryInsecticide resistance in agricultural pests challenges food security, environmental sustainability, and human health. The cotton bollworm Helicoverpa armigera is resistant to various insecticide classes as well as Bacillus thuringiensis toxins. Understanding the genetic basis of this resistance is crucial for developing effective insecticide resistance management (IRM) strategies. Our study investigated the genetic architecture of resistance of H. armigera to flubendiamide and identified SNPs associated with resistance. We used two approaches: association mapping in wild-derived samples and QTL mapping in a controlled backcross of susceptible and resistant laboratory strains. One specific region on chromosome 2 was found in both GWAS and QTL mapping analysis and showed significant potential as a PCR-based marker for monitoring resistance to flubendiamide in H. armigera. Additionally, the GWAS identified five more SNPs in the field populations. The candidate genes identified are primarily associated with insecticide detoxification mechanisms and calcium homeostasis. Our study advances the understanding of the complex genetic architecture of flubendiamide resistance in H. armigera, providing valuable tools for IRM programs and establishing a basis for future studies.

genetics↗

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

Insect crop pests threaten global food security. This threat is amplified through the spread of non-native species and the evolution of pesticide resistance, which can be introduced to a population though de novo mutation or gene flow. We investigate these processes in an economically important noctuid crop pest, Helicoverpa zea, which has rapidly evolved resistance to several pesticides. Its sister species Helicoverpa armigera, first detected as an invasive species in Brazil in 2013, introduced the pyrethroid resistance gene CYP337B3 to South American H. zea via introgression. To understand whether this contributes to pesticide resistance in North America, we sequenced 237 H. zea genomes across 10 sample sites in the US. First, we report H. armigera introgression into the North American H. zea population. Two individuals sampled in Texas in 2019 carry H. armigera haplotypes in a 4Mbp region containing CYP337B3. Second, we show that the remarkable dispersal ability of H. zea results in a panmictic North American population. Third, we detect signatures of selection in non-admixed H. zea, identifying a selective sweep at a second pesticide resistance locus with a similar name: CYP333B3. We estimate that its derived allele conferred a [~]4.9% fitness advantage and show that this estimate explains independently observed rare nonsynonymous CYP333B3 mutations approaching fixation over a [~]20-year period. We also detect putative signatures of selection at a kinesin gene associated with Bt resistance. Our results show that pesticide resistance in H. zea evolved rapidly and recently via two independent mechanisms: interspecific introgression and rapid intraspecific adaptation.

evolutionary biology↗

A framework to quantify phenotypic and genotypic parallel evolution

The independent and repeated adaptation of populations to similar environments often results in the evolution of similar forms. This phenomenon creates a strong correlation between phenotype and environment and is referred to as parallel evolution. However, we are still largely unaware of the dynamics of parallel evolution, as well as the interplay between phenotype and genotype within natural systems. Here, we examined phenotypic and genotypic parallel evolution in multiple parapatric Dune-Headland coastal ecotypes of an Australian wildflower, Senecio lautus. We observed a clear trait-environment association within the system, with all replicate populations having evolved along the same phenotypic evolutionary trajectory. Similar phenotypes have arisen via mutational changes occurring in different genes, although many share the same biological functions. Our results shed light on how replicated adaptation manifests at the phenotypic and genotypic levels within populations, and highlights S. lautus as one of the most striking cases of phenotypic parallel evolution in nature.

evolutionary biology↗

Adaptive introgression across semipermeable species boundaries between local Helicoverpa zea and invasive Helicoverpa armigera moths

Hybridization between invasive and native species has raised global concern given the dramatic increase in species range shifts and pest outbreaks due to climate change, development of suitable agroecosystems, and anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013, and more recent populations from 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, admixture proportions were reduced between 2013 and 2017, indicating a decline in hybridization rates. Recent populations also showed shorter introgressed tracks suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for introgression of a single region including an insecticide-resistance allele from the invasive H. armigera into local H. zea, which increased in frequency over time but was localized within the genome. In summary, despite extensive gene-flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression and hybridization, with significant implications for pest management in future population expansions and introductions of novel resistance genes from new invasive H. armigera populations. Author summarySecondary contact occurs when related species with non-overlapping ranges are geographically reunited. Scenarios of secondary contact have increased due to anthropogenic movement of species outside of their native range, often resulting in invasive species that successfully spread and stabilised in the new environment. This is the case for Helicoverpa armigera, a major agricultural pest in the Old World that has recently invaded the Americas, where it reunited with its closest relative, H. zea. While some authors reported hybridisation, and hypothesised about the potential emergence of novel ecotypes and the exchange of pesticide-resistant genes, these outcomes have not been tested yet. We examine these outcomes by sequencing individuals from both species in Brazil, collected in 2013 after outbreaks of H. armigera were reported, and individuals collected during 2017. We discovered that despite hybridisation, these moths have not collapsed into a single species nor formed new ecotypes, and that the species distinctiveness is maintained through selection against most of the foreign genotypes that cross species boundaries. However, we found that hybridisation mediated the rapid acquisition of a H. armigera gene conferring resistance to pyrethroids by H. zea. The overall decline in populations of both species during the interval covered by this study means that our results are likely to reflect the consequences of hybridization events early after invasion, despite the likely ongoing introduction of H. armigera genetic diversity through trade across the South American continent. Our results provide a rare example of adaptive transferral of variation right after invasion and elucidate the dynamics of insecticide resistance evolution in H. zea.

evolutionary biology↗