in

Microsatellites reveal that genetic mixing commonly occurs between invasive fall armyworm populations in Africa

  • 1.

    CABI. Fall Armyworm (FAW) Portal. www.cabi.org/isc/fallarmyworm (2020).

  • 2.

    Westbrook, J., Nagoshi, R., Meagher, R., Fleischer, S. & Jairam, S. Modeling seasonal migration of fall armyworm moths. Int. J. Biometeorol. 60, 255–267. https://doi.org/10.1007/s00484-015-1022-x (2016).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 3.

    Nagoshi, R. & Meagher, R. Review of fall armyworm (Lepidoptera: noctuidae) genetic complexity and migration. Fla. Entomol. 91, 546–554. https://doi.org/10.1653/0015-4040-91.4.546 (2008).

    Article 

    Google Scholar 

  • 4.

    Nagoshi, R. N., Meagher, R. L. & Jenkins, D. A. Puerto Rico fall armyworm has only limited interactions with those from Brazil or Texas but could have substantial exchanges with Florida populations. J. Econ. Entomol. 103, 360–367. https://doi.org/10.1603/EC09253 (2010).

    Article 
    PubMed 

    Google Scholar 

  • 5.

    Johnson, S. J. Migration and the life history strategy of the fall armyworm, Spodoptera frugiperda in the western hemisphere. Int. J. Trop. Insect Sci. 8, 543–549. https://doi.org/10.1017/S1742758400022591 (1987).

    Article 

    Google Scholar 

  • 6.

    Abrahams, P. et al. Fall Armyworm: Impacts and Implications for Africa. Evidence Note 2 (CABI, 2017).

    Google Scholar 

  • 7.

    Nagoshi, R. N. et al. Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations. PLoS ONE 12, e0171743. https://doi.org/10.1371/journal.pone.0171743 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 8.

    Arias, O. et al. Population genetic structure and demographic history of Spodoptera frugiperda (Lepidoptera: Noctuidae): Implications for insect resistance management programs. Pest Manag. Sci. 75, 2948–2957. https://doi.org/10.1002/ps.5407 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 9.

    Nagoshi, R. et al. Analysis of strain distribution, migratory potential, and invasion history of fall armyworm populations in northern Sub-Saharan Africa. Sci. Rep. 8, 3710–3710. https://doi.org/10.1038/s41598-018-21954-1 (2018).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Nagoshi, R. N., Adamczyk, J. J., Meagher, R. L., Gore, J. & Jackson, R. Using stable isotope analysis to examine fall armyworm (Lepidoptera: Noctuidae) host strains in a cotton habitat. J. Econ. Entomol. 100, 1569. https://doi.org/10.1603/0022-0493(2007)100[1569:USIATE]2.0.CO2 (2007).

    Article 
    PubMed 

    Google Scholar 

  • 11.

    Nagoshi, R. N. et al. Southeastern Asia fall armyworms are closely related to populations in Africa and India, consistent with common origin and recent migration. Sci. Rep. 10, 1421. https://doi.org/10.1038/s41598-020-58249-3 (2020).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    Nagoshi, R. N. et al. Genetic characterization of fall armyworm infesting South Africa and India indicate recent introduction from a common source population. PLoS ONE 14, e0217755. https://doi.org/10.1371/journal.pone.0217755 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 13.

    Nayyar, N. et al. Population structure and genetic diversity of invasive Fall Armyworm after 2 years of introduction in India. Sci. Rep. 11, 7760. https://doi.org/10.1038/s41598-021-87414-5 (2021).

    ADS 
    MathSciNet 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Zhang, L. et al. Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Mol. Ecol. Resour. 20, 1682–1696. https://doi.org/10.1111/1755-0998.13219 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Raymond, L., Plantegenest, M. & Vialatte, A. Migration and dispersal may drive to high genetic variation and significant genetic mixing: The case of two agriculturally important, continental hoverflies (E. pisyrphus balteatus and S. phaerophoria scripta). Mol. Ecol. 22, 5329–5339. https://doi.org/10.1111/mec.12483 (2013).

    Article 
    PubMed 

    Google Scholar 

  • 16.

    Stevens, L. et al. Migration and gene flow among domestic populations of the Chagas insect vector Triatoma dimidiata (Hemiptera: Reduviidae) detected by microsatellite loci. J. Med. Entomol. 52, 419–428. https://doi.org/10.1093/jme/tjv002 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Arias, R. S., Blanco, C. A., Portilla, M., Snodgrass, G. L. & Scheffler, B. E. First microsatellites from Spodoptera frugiperda (Lepidoptera: Noctuidae) and their potential use for population genetics. Ann. Entomol. Soc. Am. 104, 576–587. https://doi.org/10.1603/an10135 (2011).

    CAS 
    Article 

    Google Scholar 

  • 18.

    Pavinato, V. A., Martinelli, S., de Lima, P. F., Zucchi, M. I. & Omoto, C. Microsatellite markers for genetic studies of the fall armyworm, Spodoptera frugiperda. Genet. Mol. Res.: GMR https://doi.org/10.4238/2013.February.8.1 (2013).

    Article 
    PubMed 

    Google Scholar 

  • 19.

    Nagoshi, R., Silvie, P. & Meagher, R. Comparison of haplotype frequencies differentiate fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Florida and Brazil. J. Econ. Entomol. 100, 954–961 (2007).

    Article 

    Google Scholar 

  • 20.

    Agapow, P.-M. & Burt, A. Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1, 101–102. https://doi.org/10.1046/j.1471-8278.2000.00014.x (2001).

    CAS 
    Article 

    Google Scholar 

  • 21.

    Weir, B. S. Genetic Data Analysis II: Methods for Discrete Population Genetic Data (Sinauer, 1996).

    Google Scholar 

  • 22.

    Nei, M. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. 70, 3321. https://doi.org/10.1073/pnas.70.12.3321 (1973).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • 23.

    Hedrick, P. W. A standardized genetic differentiation measure. Evolution 59, 1633–1638. https://doi.org/10.1111/j.0014-3820.2005.tb01814.x (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 24.

    Jost, L. O. U. GST and its relatives do not measure differentiation. Mol. Ecol. 17, 4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x (2008).

    Article 
    PubMed 

    Google Scholar 

  • 25.

    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software structure: A simulation study. Mol. Ecol. 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 26.

    Jombart, T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405. https://doi.org/10.1093/bioinformatics/btn129 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 27.

    Nagoshi, R. N. et al. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS ONE 12, e0181982. https://doi.org/10.1371/journal.pone.0181982 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 28.

    Nagoshi, R. N., Goergen, G., Plessis, H. D., van den Berg, J. & Meagher, R. Genetic comparisons of fall armyworm populations from 11 countries spanning sub-Saharan Africa provide insights into strain composition and migratory behaviors. Sci. Rep. 9, 8311. https://doi.org/10.1038/s41598-019-44744-9 (2019).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 29.

    Buès, R., Bouvier, J. C. & Boudinhon, L. Insecticide resistance and mechanisms of resistance to selected strains of Helicoverpa armigera (Lepidoptera: Noctuidae) in the south of France. Crop Prot. 24, 814–820. https://doi.org/10.1016/j.cropro.2005.01.006 (2005).

    CAS 
    Article 

    Google Scholar 

  • 30.

    Armes, N. J., Jadhav, D. R. & DeSouza, K. R. A survey of insecticide resistance in Helicoverpa armigera in the Indian subcontinent. Bull. Entomol. Res. 86, 499–514. https://doi.org/10.1017/S0007485300039298 (1996).

    CAS 
    Article 

    Google Scholar 

  • 31.

    Parry, H. R. et al. Estimating the landscape distribution of eggs by Helicoverpa spp., with implications for Bt resistance management. Ecol. Model. 365, 129–140. https://doi.org/10.1016/j.ecolmodel.2017.10.004 (2017).

    Article 

    Google Scholar 

  • 32.

    Jones, C. M., Parry, H., Tay, W. T., Reynolds, D. R. & Chapman, J. W. Movement ecology of pest Helicoverpa: Implications for ongoing spread. Annu. Rev. Entomol. 64, 277–295. https://doi.org/10.1146/annurev-ento-011118-111959 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 33.

    Tucker, M. R., Mwandoto, S. & Pedgley, D. E. Further evidence for windborne movement of armyworm moths, Spodoptera exempta, in East Africa. Ecol. Entomol. 7, 463–473. https://doi.org/10.1111/j.1365-2311.1982.tb00689.x (1982).

    Article 

    Google Scholar 

  • 34.

    Rose, D. J. W. et al. Downwind migration of the African army worm moth, Spodoptera exempta, studied by mark-and-capture and by radar. Ecol. Entomol. 10, 299–313. https://doi.org/10.1111/j.1365-2311.1985.tb00727.x (1985).

    Article 

    Google Scholar 

  • 35.

    Rose, D. J. W., Dewhurst, C. F. & Page, W. W. The African Armyworm Handbook: The Status, Biology, Ecology, Epidemiology and Management of Spodoptera exempta (Lepidoptera: Noctuidae) (Natural Resources Institute, 2000).

    Google Scholar 

  • 36.

    Chapman, J. W., Reynolds, D. R. & Wilson, K. Long-range seasonal migration in insects: Mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 18, 287–302. https://doi.org/10.1111/ele.12407 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 37.

    Nagoshi, R. N. & Meagher, R. L. Using intron sequence comparisons in the triose-phosphate isomerase gene to study the divergence of the fall armyworm host strains. Insect Mol. Biol. 25, 324–337. https://doi.org/10.1111/imb.12223 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 38.

    Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acid Symp. Ser. 41, 95–98 (1999).

    CAS 

    Google Scholar 

  • 39.

    Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673–4680. https://doi.org/10.1093/nar/22.22.4673 (1994).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    R Core Team. R Foundation for Statistical Computing (R Core Team, 2020).

    Google Scholar 

  • 41.

    Paradis, E. pegas: An R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420. https://doi.org/10.1093/bioinformatics/btp696 (2010).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 42.

    Adamack, A. & Gruber, B. PopGenReport: Simplifying basic population genetic analyses in R. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.12158 (2014).

    Article 

    Google Scholar 

  • 43.

    Goudet, J. Hierfstat, a package for r to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x (2005).

    Article 

    Google Scholar 

  • 44.

    Winter, D. MMOD: An R library for the calculation of population differentiation statistics. Mol. Ecol. Resour. https://doi.org/10.1111/j.1755-0998.2012.03174.x (2012).

    Article 
    PubMed 

    Google Scholar 

  • 45.

    Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. https://doi.org/10.7717/peerj.281 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Raymond, M. & Rousset, F. GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573 (1995).

    Article 

    Google Scholar 

  • 47.

    Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.0-2. (2012).

  • 48.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS 
    Article 

    Google Scholar 

  • 49.

    Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).

    Article 

    Google Scholar 

  • 50.

    Jakobsson, M. & Rosenberg, N. A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806. https://doi.org/10.1093/bioinformatics/btm233 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 51.

    Rosenberg, N. A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x (2004).

    Article 

    Google Scholar 

  • High canopy cover of invasive Acer negundo L. affects ground vegetation taxonomic richness

    The invasive cactus Opuntia stricta creates fertility islands in African savannas and benefits from those created by native trees