Two host-plant strains in the fall armyworm

Abstract

The fall armyworm (Spodoptera frugiperda) is one of the major pest insects damaging diverse crops including cotton, corn, rice, and sorghum. Fall armyworms have been identified as two morphologically indistinguishable strains, the corn strain, and the rice strain, named after their preferred host-plants. Although initially recognized as host-plant strains, there has been an ongoing debate regarding whether the corn and rice strains should be considered as such. In this article, we present arguments based on recent population genomics studies supporting that these two strains should be considered to be host-plant strains. Furthermore, host-plant adaptation appears to be a driving evolutionary force responsible for incipient speciation in the fall armyworm.

Keywords

fall armyworm / host-plant adaptation / incipient speciation / Spodoptera frugiperda

References

[1] Bai-Zhong, Z.,Xu, S.,Cong-Ai, Z.,Liu-Yang, L.,Ya-She, L.,Xing, G. et al. (2020) Silencing of Cytochrome P450 in Spodoptera frugiperda (Lepidoptera: Noctuidae) by RNA interference enhances susceptibility to chlorantraniliprole. Journal of Insect Science,20,12.

[2] Barton, N.H. (1979) Gene flow past a cline. Heredity,43,333–339.

[3] Barton, N.H. (1983) Multilocus clines. Evolution; International Journal of Organic Evolution,37,454–471.

[4] Blanco, C.A.,Portilla, M.,Jurat-Fuentes, J.L.,Sánchez, J.F.,Viteri, D.,Vega-Aquino, P., et al. (2010) Susceptibility of isofamilies of Spodoptera frugiperda (Lepidoptera: Noctuidae) to Cry1Ac and Cry1Fa proteins of Bacillus thuringiensis. Southwestern Entomologist,35,409–416.

[5] Cañas-Hoyos, N.,Lobo-Echeverri, T. and Saldamando-Benjumea, C.I. (2017) Chemical composition of female sexual glands of Spodoptera frugiperda corn and rice strains from Tolima, Colombia. Southwestern Entomologist,42,375–394.

[6] Cañas-Hoyos, N.,Márquez, E.J. and Saldamando-Benjumea, C.I. (2014) Differentiation of Spodoptera frugiperda (Lepidoptera: Noctuidae) corn and rice strains from central Colombia: a wing morphometric approach. Annals of the Entomological Society of America,107,575–581.

[7] Chandrasena, D.I.,Signorini, A.M.,Abratti, G.,Storer, N.P.,Olaciregui, M.L.,Alves, A.P. et al. (2018) Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina. Pest Management Science,74,746–754.

[8] Day, R.,Abrahams, P.,Bateman, M.,Beale, T.,Clottey, V.,Cock, M. et al. (2017) Fall armyworm: impacts and implications for Africa. Outlooks on Pest Management,28,196–201.

[9] Drès, M. and Mallet, J. (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences,357,471–492.

[10] Dumas, P.,Legeai, F.,Lemaitre, C.,Scaon, E.,Orsucci, M.,Labadie, K. et al. (2015) Spodoptera frugiperda (Lepidoptera: Noctuidae) host-plant variants: Two host strains or two distinct species? Genetica,143,305–316.

[11] Feder, J.L.,Egan, S. and Nosil, P. (2012a) The genomics of speciation-with-gene-flow. Trends in Genetics,28,342–350.

[12] Feder, J.L.,Gejji, R.,Yeaman, S. and Nosil, P. (2012b) Establishment of new mutations under divergence and genome hitchhiking. Philosophical Transactions of the Royal Society B: Biological Sciences,367,461–474.

[13] Feder, J.L. and Nosil, P. (2010) The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution; International Journal of Organic Evolution,64,1729–1747.

[14] Felsenstein, J. (1981) Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution; International Journal of Organic Evolution,35,124–138.

[15] Fiteni, E.,Durand, K.,Gimenez, S.,Meagher, R.L.,Legeai, F.,Kergoat, G.J. et al. (2022) Host-plant adaptation as a driver of incipient speciation in the fall armyworm (Spodoptera frugiperda). BMC Ecology and Evolution,22,133.

[16] Flaxman, S.M.,Wacholder, A.C.,Feder, J.L. and Nosil, P. (2014) Theoretical models of the influence of genomic architecture on the dynamics of speciation. Molecular Ecology,23,4074–4088.

[17] Goergen, G.,Kumar, P.L.,Sankung, S.B.,Togola, A. and Tamò 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.

[18] Gouin, A.,Bretaudeau, A.,Nam, K.,Gimenez, S.,Aury, J.M.,Duvic, B. et al. (2017) Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges. Scientific Reports,7,11816.

[19] Groot, A.T.,Marr, M.,Schöfl, G.,Lorenz, S.,Svatos, A. and Heckel, D.G. (2008) Host strain specific sex pheromone variation in Spodoptera frugiperda. Frontiers in Zoology,5,1.

[20] Guan, F.,Zhang, J.,Shen, H.,Wang, X.,Padovan, A.,Walsh, T.K. et al. (2021) Whole-genome sequencing to detect mutations associated with resistance to insecticides and Bt proteins in Spodoptera frugiperda. Insect Science,28,627–638.

[21] Gui, F.,Lan, T.,Zhao, Y.,Guo, W.,Dong, Y.,Fang, D. et al. (2020) Genomic and transcriptomic analysis unveils population evolution and development of pesticide resistance in fall armyworm Spodoptera frugiperda. Protein & Cell,13,513–531.

[22] Hänniger, S.,Dumas, P.,Schöfl, G.,Gebauer-Jung, S.,Vogel, H.,Unbehend, M. et al. (2017) Genetic basis of allochronic differentiation in the fall armyworm. BMC Evolutionary Biology,17,68.

[23] Hendrich, L.,Pons, J.,Ribera, I. and Balke, M. (2010) Mitochondrial cox1 sequence data reliably uncover patterns of insect diversity but suffer from high lineage-idiosyncratic error rates. PLoS ONE,5,e14448.

[24] Herlinda, S.,Suharjo, R.,Elbi Sinaga, M.,Fawwazi, F. and Suwandi, S. (2022) First report of occurrence of corn and rice strains of fall armyworm,Spodoptera frugiperda in South Sumatra, Indonesia and its damage in maize. Journal of the Saudi Society of Agricultural Sciences,21,412–419.

[25] Hill, G.E. (2015) Mitonuclear ecology. Molecular Biology and Evolution,32,1917–1927.

[26] Juárez, M.L.,Murúa, M.G.,García, M.G.,Ontivero, M.,Vera, M.T.,Vilardi, J.C. et al. (2012) Host association of Spodoptera frugiperda (Lepidoptera: Noctuidae) corn and rice strains in Argentina, Brazil, and Paraguay. Journal of Economic Entomology,105,573–582.

[27] Kergoat, G.J.,Prowell, D.P.,Le Ru, B.P.,Mitchell, A.,Dumas, P.,Clamens, A.L. et al. (2012) Disentangling dispersal, vicariance and adaptive radiation patterns: a case study using armyworms in the pest genus Spodoptera (Lepidoptera: Noctuidae). Molecular Phylogenetics and Evolution,65,855–870.

[28] Kim, H.G.,Park, J.S. and Lee, D.H. (2018) Potential of unmanned aerial sampling for monitoring insect populations in rice fields. Florida Entomologist,101,330–334.

[29] Lima, E.R. and McNeil, J.N. (2009) Female sex pheromones in the host races and hybrids of the fall armyworm,Spodoptera frugiperda (Lepidoptera: Noctuidae). Chemoecology,19,29–36.

[30] Lu, Y.J.,Kochert, G.D.,Isenhour, D.J. and Adang, M.J. (1994) Molecular characterization of a strain-specific repeated DNA sequence in the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insect Molecular Biology,3,123–130.

[31] Lv, S.L.,Shi, Y.,Zhang, J.C.,Liang, P.,Zhang, L. and Gao, X.W. (2021) Detection of ryanodine receptor target-site mutations in diamide insecticide-resistant Spodoptera frugiperda in China. Insect Science,28,639–648.

[32] Montezano, D.G.,Specht, A.,Sosa-Gómez, D.R.,Roque-Specht, V.F.,Sousa-Silva, J.C.,Paula-Moraes, S.V. et al. (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology,26,286–300.

[33] Nagoshi, K.L.,Allan, S.A. and Meagher, R.L. (2020) Assessing the use of wing morphometrics to identify fall armyworm (Lepidoptera: Noctuidae) host strains in field collections. Journal of Economic Entomology,113,800–807.

[34] Nagoshi, R.N. (2010) The fall armyworm Triosephosphate Isomerase (Tpi) gene as a marker of strain identity and interstrain mating. Annals of the Entomological Society of America,103,283–292.

[35] Nagoshi, R.N.,Goergen, G.,Koffi, D.,Agboka, K.,Adjevi, A.K.M.,Du Plessis, H. et al. (2022) Genetic studies of fall armyworm indicate a new introduction into Africa and identify limits to its migratory behavior. Scientific Reports,12,1941.

[36] Nagoshi, R.N.,Goergen, G.,Plessis, H.D.,van den Berg, J. and Meagher, R. (2019) Genetic comparisons of fall armyworm populations from 11 countries spanning sub-Saharan Africa provide insights into strain composition and migratory behaviors. Scientific Reports,9,8311.

[37] Nagoshi, R.N.,Koffi, D.,Agboka, K.,Adjevi, A.K.M.,Meagher, R.L. and Goergen, G. (2021) The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo. PLoS ONE,16,e0253528.

[38] Nagoshi, R.N.,Koffi, D.,Agboka, K.,Tounou, K.A.,Banerjee, R.,Jurat-Fuentes, J.L. et al. (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.

[39] Nagoshi, R.N. and Meagher, R.L. (2022) The Spodoptera frugiperda host strains: What they are and why they matter for understanding and controlling this global agricultural pest. Journal of Economic Entomology,115,1729–1743.

[40] Nam, K.,Nhim, S.,Robin, S.,Bretaudeau, A.,Nègre, N. and d’Alençon, E. (2020) Positive selection alone is sufficient for whole genome differentiation at the early stage of speciation process in the fall armyworm. BMC Evolutionary Biology,20,152.

[41] Navasero, M.M.,Navasero, M.V.,Aquino, M.F.G. and Navasero, J.M. (2023) Morphological, molecular and biological characterization of Spodoptera frugiperda (JE Smith) from Rice in Northern Luzon, Philippines. International Journal of Agricultural Technology,19,1149–1164.

[42] Nosil, P.,Crespi, B.J. and Sandoval, C.P. (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature,417,440–443.

[43] Nuss, E.T. and Tanumihardjo, S.A. (2010) Maize: a paramount staple crop in the context of global nutrition. Comprehensive Reviews in Food Science and Food Safety,9,417–436.

[44] Orsucci, M.,Moné Y.,Audiot, P.,Gimenez, S.,Nhim, S.,Naït-Saïdi, R. et al. (2022) Transcriptional differences between the two host strains of Spodoptera frugiperda (Lepidoptera: Noctuidae). Peer Community Journal,2,e1.

[45] Pashley, D.P. (1986) Host-associated genetic differentiation in fall armyworm (Lepidoptera: Noctuidae): a sibling species complex? Annals of the Entomological Society of America,79,898–904.

[46] Pashley, D.P. (1988) Current status of fall armyworm host strains. The Florida Entomologist,71,227–234.

[47] Pashley, D.P. (1989) Host-associated differentiation in armyworms (Lepidoptera: Noctuidae): an allozymic and mtDNA perspective. In Electrophoretic Studies on Agricultural Pests (eds. H.D. Loxdale & J.D. Hollander), pp. 103–114. Clarendon Press.

[48] Pashley, D.P.,Hammond, A.M. and Hardy, T.N. (1992) Reproductive isolating mechanisms in fall armyworm host strains (Lepidoptera: Noctuidae). Annals of the Entomological Society of America,85,400–405.

[49] Pashley, D.P. and Martin, J.A. (1987) Reproductive incompatibility between host strains of the fall armyworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America,80,731–733.

[50] Prowell, D.P.,McMichael, M. and Silvain, J.F. (2004) Multilocus genetic analysis of host use, introgression, and speciation in host strains of fall armyworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America,97,1034–1044.

[51] Rwomushana, I. (2019) Spodoptera frugiperda (fall armyworm). CABI Compendium; CABI International. https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.29810

[52] Saldamando-Benjumea, C.I.,Estrada-Piedrahíta, K.,Velásquez-Vélez, M.I. and Bailey, R.I. (2014) Assortative mating and lack of temporality between corn and rice strains of Spodoptera frugiperda (Lepidoptera, Noctuidae) from Central Colombia. Journal of Insect Behavior,27,555–566.

[53] Schöfl, G.,Dill, A.,Heckel, D.G.,Groot, A.T.,Boughman, A.E.J. and McPeek, E.M.A. (2011) Allochronic separation versus mate choice: nonrandom patterns of mating between fall armyworm host strains. The American Naturalist,177,470–485.

[54] Schöfl, G.,Heckel, D.G. and Groot, A.T. (2009) Time-shifted reproductive behaviours among fall armyworm (Noctuidae: Spodoptera frugiperda) host strains: evidence for differing modes of inheritance. Journal of Evolutionary Biology,22,1447–1459.

[55] Smith, J.M. and Haigh, J. (1974) The hitch-hiking effect of a favourable gene. Genetical Research,23,23–35.

[56] Storer, N.P.,Babcock, J.M.,Schlenz, M.,Meade, T.,Thompson, G.D.,Bing, J.W. et al. (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology,103,1031–1038.

[57] Tessnow, A.E.,Raszick, T.J.,Porter, P. and Sword, G.A. (2022) Patterns of genomic and allochronic strain divergence in the fall armyworm,Spodoptera frugiperda (J E Smith). Ecology and Evolution,12,e8706.

[58] Unbehend, M.,Hänniger, S.,Meagher, R.L.,Heckel, D.G. and Groot, A.T. (2013) Pheromonal divergence between two strains of Spodoptera frugiperda. Journal of Chemical Ecology,39,364–376.

[59] Unbehend, M.,Hänniger, S.,Vásquez, G.M.,Juárez, M.L.,Reisig, D.,McNeil, J.N. et al. (2014) Geographic variation in sexual attraction of Spodoptera frugiperda corn-and rice-strain males to pheromone lures. PLoS ONE,9,e89255.

[60] Velásquez-Vélez, M.I.,Saldamando-Benjumea, C.I. and Ríos-Diez, J.D. (2011) Reproductive isolation between two populations of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected in corn and rice fields from Central Colombia. Annals of the Entomological Society of America,104,826–833.

[61] Yainna, S.,Tay, W.T.,Durand, K.,Fiteni, E.,Hilliou, F.,Legeai, F. et al. (2022) The evolutionary process of invasion in the fall armyworm (Spodoptera frugiperda). Scientific Reports,12,21063.

[62] Yamamoto, K.,Nohata, J.,Kadono-Okuda, K.,Narukawa, J.,Sasanuma, M.,Sasanuma, S. et al. (2008) A BAC-based integrated linkage map of the silkworm Bombyx mori. Genome Biology,9,R21.

[63] Yousaf, S.,Rehman, A.,Masood, M.,Ali, K. and Suleman, N. (2022) Occurrence and molecular identification of an invasive rice strain of fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) from Sindh, Pakistan, using mitochondrial cytochrome c oxidase I gene sequences. Journal of Plant Diseases and Protection,129,71–78.

[64] Zhang, D.,Xiao, Y.,Xu, P.,Yang, X.,Wu, Q. and Wu, K. (2021) Insecticide resistance monitoring for the invasive populations of fall armyworm,Spodoptera frugiperda in China. Journal of Integrative Agriculture,20,783–791.

[65] Zhao, Y.X.,Huang, J.M.,Ni, H.,Guo, D.,Yang, F.X.,Wang, X. et al. (2020) Susceptibility of fall armyworm,Spodoptera frugiperda (J.E. Smith), to eight insecticides in China, with special reference to lambda-cyhalothrin. Pesticide Biochemistry and Physiology,168,104623.

RIGHTS & PERMISSIONS

2024 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.