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Population genetics reveal multiple independent invasions of Spodoptera frugiperda (Lepidoptera: Noctuidae) in China

Published online by Cambridge University Press:  28 April 2022

Yun-Yuan Jiang ,
Yi-Yin Zhang ,
Xin-Yu Zhou ,
Xiao-Yue Hong Open the ORCID record for Xiao-Yue Hong [Opens in a new window]  and
Lei Chen Open the ORCID record for Lei Chen [Opens in a new window]
Yun-Yuan Jiang
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Yi-Yin Zhang
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Xin-Yu Zhou
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Xiao-Yue Hong
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Lei Chen*
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
*
Author for correspondence: Lei Chen, Email: [email protected]
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Abstract

The fall armyworm (Spodoptera frugiperda), a destructive pest that originated in South and North America, spread to China in early 2019. Controlling this invasive pest requires an understanding of its population structure and migration patterns, yet the invasion genetics of Chinese S. frugiperda is not clear. Here, using the mitochondrial cytochrome oxidase subunit I (COI) gene, triose phosphate isomerase (Tpi) gene and eight microsatellite loci, we investigated genetic structure and genetic diversity of 16 S. frugiperda populations in China. The Tpi locus identified most S. frugiperda populations as the corn-strains, and a few were heterozygous strains. The microsatellite loci revealed that the genetic diversity of this pest in China was lower than that in South America. Furthermore, we found moderate differentiation among the populations, distinct genetic structures between adjacent populations and abundant genetic resources in the S. frugiperda populations from China sampled across 2 years. The survival rate of S. frugiperda was significantly higher when it was fed on corn leaves than on rice leaves, and the larval stage mortality rate was the highest under both treatments. Our results showed that S. frugiperda probably invaded China via multiple independent introductions and careful pesticide control, continuous monitoring and further studies will be needed to minimize its potential future outbreak.

Keywords

Genetic diversitypopulation structureSpodoptera frugiperdaSSR
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 6 , December 2022 , pp. 796 - 806
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Arias, RS, Blanco, CA, Portilla, M, Snodgrass, GL and Scheffler, BE (2011) First microsatellites from Spodoptera frugiperda (Lepidoptera: Noctuidae) and their potential use for population genetics. Annals of the Entomological Society of America 104, 576–587.CrossRefGoogle Scholar
Arias, O, Cordeiro, E, Correa, AS, Domingues, FA, Guidolin, AS and Omoto, C (2019) Population genetic structure and demographic history of Spodoptera frugiperda (Lepidoptera: Noctuidae): implications for insect resistance management programs. Pest Management Science 75, 2948–2957.CrossRefGoogle ScholarPubMed
Behura, SK (2006) Molecular marker systems in insects: current trends and future avenues. Molecular Ecology 15, 3087–3113.CrossRefGoogle ScholarPubMed
Bentivenha, JPF, Montezano, DG, Hunt, TE, Baldin, ELL, Peterson, JA, Victor, VS, Pannuti, LER, Velez, AM and Paula-Moraes, SV (2017) Intraguild interactions and behavior of Spodoptera frugiperda and Helicoverpa spp. on maize. Pest Management Science 73, 2244–2251.CrossRefGoogle ScholarPubMed
Busato, GR, Grutzmacher, AD, Garcia, MS, Giolo, FP, Zotti, MJ and Stefanello, J (2005) Compared biology of Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) populations in corn and rice leaves. Neotropical Entomology 34, 743–750.CrossRefGoogle Scholar
Casmuz, A, Laura-Juarez, M, Guillermina-Socias, M, Gabriela-Murua, M, Prieto, S, Medina, S, Willink, E and Gastaminza, G (2010) Review of the host plants of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Revista de la Sociedad Entomologica Argentina 69, 209–231.Google Scholar
Centre Agriculture Bioscience International (CABI) (2019) Datasheet Spodoptera frugiperda (fall armyworm). Invasive Species Compendium, Available at https://www.cabi.org/isc/datasheet/29810#94987198-9f50-4173-8bbd30bd93840e73?tdsourcetag=s_pcqq_aiomsg (Accessed 26 April 2019).Google Scholar
Chen, MH and Dorn, S (2010) Microsatellites reveal genetic differentiation among populations in an insect species with high genetic variability in dispersal, the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Bulletin of Entomological Research 100, 75–85.CrossRefGoogle Scholar
Chen, H, Wu, MF, Liu, J, Chen, AD, Jiang, YY and Hu, G (2020a) Migratory routes and occurrence divisions of the fall armyworm Spodoptera frugiperda in China. Plant Protection 47, 747–757.Google Scholar
Chen, H, Yang, XL, Zhan, AD, Li, YC, Wang, DH, Liu, J and Hu, G (2020b) Immigration timing and origin of the first fall armyworms (Spodoptera frugiperda) detected in China. Chinese Journal of Applied Entomology 57, 1270–1278.Google Scholar
Cui, ZB, Li, ZQ, Wang, Y and He, C (2020) Research status and control strategies of Spodoptera frugiperda. Hunan Agriculture Science 2020, 38–42.Google Scholar
Dingle, H (1972) Migration strategies of insects. Science (New York, N.Y.) 175, 1327–1335.CrossRefGoogle ScholarPubMed
Earl, DA and vonHoldt, BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.CrossRefGoogle Scholar
Early, R, Gonzalez-Moreno, P, Murphy, ST and Day, R (2018) Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. Neobiota 40, 25–50.CrossRefGoogle Scholar
Evanno, G, Regnaut, S and Goudet, J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.CrossRefGoogle ScholarPubMed
Exposito-Alonso, M, Becker, C, Schuenemann, VJ, Reiter, E, Setzer, C, Slovak, R, Brachi, B, Hagmann, J, Grimm, DG, Chen, J, Busch, W, Bergelson, J, Ness, RW, Krause, J, Burbano, HA and Weigel, D (2018) The rate and potential relevance of new mutations in a colonizing plant lineage. PloS Genetics 14, e1007155.CrossRefGoogle Scholar
Falush, D, Stephens, M and Pritchard, JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.CrossRefGoogle ScholarPubMed
Falush, D, Stephens, M and Pritchard, JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574–578.CrossRefGoogle ScholarPubMed
Goergen, G, Kumar, PL, Sankung, SB, Togola, A and Tamo, M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS ONE 11, e0165632.CrossRefGoogle Scholar
Goudet, J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9.3.2. Available at http://www2.unil.ch/popgen/softwares/fstat.htm.Google Scholar
Jakobsson, M and Rosenberg, NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics (Oxford, England) 23, 1801–1806.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Lee, CE (2002) Evolutionary genetics of invasive species. Trends in Ecology and Evolution 17, 386–391.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Levy, HC, Garcia-Maruniak, A and Maruniak, JE (2002) Strain identification of Spodoptera frugiperda (Lepidoptera: Noctuidae) insects and cell line: PCR-RFLP of cytochrome oxidase C subunit I gene. Florida Entomologist 85, 186–190.CrossRefGoogle Scholar
Li, XJ, Wu, MF, Ma, J, Gao, BY, Wu, QL, Chen, AD, Liu, J, Jiang, YY, Zhai, BP, Early, R, Chapman, JW and Hu, G (2020) Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Management Science 76, 454–463.CrossRefGoogle ScholarPubMed
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lu, YJ, Adang, MJ, Isenhour, DJ and Kochert, GD (1992) RFLP analysis of genetic variation in North American populations of the fall armyworm moth Spodoptera frugiperda (Lepidoptera: Noctuidae). Molecular Ecology 1, 199–207.CrossRefGoogle Scholar
Meagher, RL and Nagoshi, RN (2004) Population dynamics and occurrence of Spodoptera frugiperda host strains in southern Florida. Ecological Entomology 29, 614–620.CrossRefGoogle Scholar
Ministry of Agriculture and Rural Affairs of the People's Republic of China (MARA) (2019) Ministry of Agriculture and Rural Affairs held a press conference on the prevention and control of Spodoptera frugiperda. Available at http://www.moa.gov.cn/hd/zbft_news/cdtyefk/ (Accessed 17 September 2019).Google Scholar
Nagoshi, RN (2010) The fall armyworm Triose Phosphate Isomerase (Tpi) gene as a marker of strain identity and interstrain mating. Annals of the Entomological Society of America 103, 283–292.CrossRefGoogle Scholar
Nagoshi, RN (2012) Improvements in the identification of strains facilitate population studies of fall armyworm subgroups. Annals of the Entomological Society of America 105, 351–358.CrossRefGoogle Scholar
Nagoshi, RN and Meagher, RL (2004) Seasonal distribution of fall armyworm (Lepidoptera: Noctuidae) host strains in agricultural and turf grass habitats. Environmental Entomology 33, 881–889.CrossRefGoogle Scholar
Nagoshi, RN and Meagher, RL (2016) Using intron sequence comparisons in the Triosephosphate isomerase gene to study the divergence of the fall armyworm host strains. Insect Molecular Biology 25, 324–337.CrossRefGoogle Scholar
Nagoshi, RN, Silvie, P and Meagher, RL (2007a) Comparison of haplotype frequencies differentiate fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Florida and Brazil. Journal of Economic Entomology 100, 954–961.CrossRefGoogle ScholarPubMed
Nagoshi, RN, Silvie, P, Meagher, RL, Lopez, J and Machados, V (2007b) Identification and comparison of fall armyworm (Lepidoptera: Noctuidae) host strains in Brazil, Texas, and Florida. Annals of the Entomological Society of America 100, 394–402.CrossRefGoogle Scholar
Nagoshi, RN, Meagher, RL and Hay-Roe, M (2012) Inferring the annual migration patterns of fall armyworm (Lepidoptera: Noctuidae) in the United States from mitochondrial haplotypes. Ecology and Evolution 2, 1458–1467.CrossRefGoogle ScholarPubMed
Nagoshi, RN, Koffi, D, Agboka, K, Tounou, KA, Banerjee, R, Jurat-Fuentes, JL and Meagher, RL (2017) 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.CrossRefGoogle ScholarPubMed
Otim, MH, Tay, WT, Walsh, TK, Kanyesigye, D, Adumo, S, Abongosi, J, Ochen, S, Sserumaga, J, Alibu, S, Abalo, G, Asea, G and Agona, A (2018) Detection of sister-species in invasive populations of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) from Uganda. PLoS ONE 13, e0194571.CrossRefGoogle ScholarPubMed
Pair, SD, Raulston, JR, Sparks, AN, Westbrook, JK and Douce, GK (1986) Fall armyworm distribution and population dynamics in the southeastern states. Florida Entomologist 69, 468–487.CrossRefGoogle Scholar
Parepa, M, Fischer, M, Krebs, C and Bossdorf, O (2014) Hybridization increases invasive knotweed success. Evolutionary Applications 7, 413–420.CrossRefGoogle ScholarPubMed
Pashley, DP and Martin, JA (1987) Reproductive incompatibility between host strains of the fall armyworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 80, 731–733.CrossRefGoogle Scholar
Pashley, DP, Johnson, SJ and Sparks, AN (1985) Genetic population structure of migratory moths: the fall armyworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 78, 756–762.CrossRefGoogle Scholar
Pavinato, VAC, Martinelli, S, de-Lima, PF, Zucchi, MI and Omoto, C (2013) Microsatellite markers for genetic studies of the fall armyworm, Spodoptera frugiperda. Genetics and Molecular Research 12, 370–380.CrossRefGoogle ScholarPubMed
Peakall, R and Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics (Oxford, England) 28, 2537–2539.CrossRefGoogle ScholarPubMed
Porretta, D, Canestrelli, D, Bellini, R, Celli, G and Urbanelli, S (2007) Improving insect pest management through population genetic data: a case study of the mosquito Ochlerotatus caspius (Pallas). Journal of Applied Ecology 44, 682–691.CrossRefGoogle Scholar
Pritchard, JK, Stephens, M and Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.CrossRefGoogle ScholarPubMed
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.CrossRefGoogle ScholarPubMed
Rosenberg, NA (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.CrossRefGoogle Scholar
Rousset, F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106.CrossRefGoogle ScholarPubMed
Sakai, AK, Allendorf, FW, Holt, JS, Lodge, DM, Molofsky, J, With, KA, Baughman, S, Cabin, RJ, Cohen, JE, Ellstrand, NC, McCauley, DE, O'Neil, P, Parker, IM, Thompson, JN and Weller, SG (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305–332.CrossRefGoogle Scholar
Sena, DG, Pinto, FAC, Queiroz, DM and Viana, PA (2003) Fall armyworm damaged maize plant identification using digital images. Biosystems Engineering 85, 449–454.CrossRefGoogle Scholar
Smith, AL, Hodkinson, TR, Villellas, J, Catford, JA, Csergo, AM, Blomberg, SP, Crone, EE, Ehrlen, J, Garcia, MB, Laine, AL, Roach, DA, Salguero-Gomez, R, Wardle, GM, Childs, DZ, Elderd, BD, Finn, A, Munne-Bosch, S, Baudraz, MEA, Bodis, J, Brearley, FQ, Bucharova, A, Caruso, CM, Duncan, RP, Dwyerh, J, Gooden, B, Groenteman, R, Hamre, LN, Helm, A, Kelly, R, Laanisto, L, Lonati, M, Moore, JL, Morales, M, Olsen, SL, Partel, M, Petry, WK, Ramula, S, Rasmussen, PU, Enri, SR, Roeder, A, Roscher, C, Saastamoinen, M, Tack, AJM, Topper, JP, Vose, GE, Wandrag, EM, Wingler, A and Buckley, YM (2020) Global gene flow releases invasive plants from environmental constraints on genetic diversity. Proceedings of the National Academy of Sciences of the United States of America 117, 4218–4227.CrossRefGoogle ScholarPubMed
Sun, JT, Jiang, XY, Wang, MM and Hong, XY (2014) Development of microsatellite markers for, and a preliminary population genetic analysis of, the white-backed planthopper. Bulletin of Entomological Research 104, 765–773.CrossRefGoogle Scholar
Valade, R, Kenis, M, Hernandez-Lopez, A, Augustin, S, Mena, NM, Magnoux, E, Rougerie, R, Lakatos, F, Roques, A and Lopez-Vaamonde, C (2009) Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera: Gracillariidae). Molecular Ecology 18, 3458–3470.CrossRefGoogle ScholarPubMed
Van-Oosterhout, C, Hutchinson, WF, Wills, DPM and Shipley, P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.CrossRefGoogle Scholar
Wei, SJ, Shi, BC, Gong, YJ, Jin, GH, Chen, XX and Meng, XF (2013) Genetic structure and demographic history reveal migration of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) from the Southern to Northern Regions of China. PLoS ONE 8, e59654.CrossRefGoogle ScholarPubMed
Westbrook, JK, Nagoshi, RN, Meagher, RL, Fleischer, SJ and Jairam, S (2016) Modeling seasonal migration of fall armyworm moths. International Journal of Biometeorology 60, 255–267.CrossRefGoogle ScholarPubMed
Westbrook, JK, Fleischer, SJ, Jairam, S, Meagher, RL and Nagoshi, RN (2019) Multigenerational migration of fall armyworm, a pest insect. Ecosphere (Washington, D.C) 10, e02919.Google Scholar
Wilson, GA and Rannala, B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163, 1177–1191.CrossRefGoogle ScholarPubMed
Wilson, JRU, Dormontt, EE, Prentis, PJ, Lowe, AJ and Richardson, DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends in Ecology and Evolution 24, 136–144.CrossRefGoogle ScholarPubMed
Wright, S (1931) Evolution in Mendelian populations. Genetics 16, 97. https://doi.org/10.1093/genetics/16.2.97.CrossRefGoogle ScholarPubMed
Wu, QL, Jiang, YY and Wu, KM (2019) Path analysis of Burmese source of Spodoptera frugiperda into China. Plant Protection 45, 1–6.Google Scholar
Wu, MF, Qi, GJ, Chen, H, Ma, J, Liu, J, Jiang, YY, Lee, GS, Otuka, A and Hu, G (2021) Overseas immigration of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), invading Korea and Japan in 2019. Insect Science 29, 505–520. https://doi.org/10.1111/1744-7917.12940.Google ScholarPubMed
Yang, XM, Sun, JT, Xue, XF, Li, JB and Hong, XY (2012) Invasion genetics of the western flower thrips in China: evidence for genetic bottleneck, hybridization and bridgehead effect. PLoS ONE 7, e34567.CrossRefGoogle ScholarPubMed
Zhang, L, Jin, MH, Zhang, DD, Jiang, YY, Liu, J and Wu, KM (2019) Molecular identification of invasive fall armyworm Spodoptera frugiperda in Yunnan province. Plant Protection 45, 19–24.Google Scholar
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