Heterosis effect for larval performance of fall armyworm interstrain hybrids.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Author(s): Lan L;Lan L; Nègre N; Nègre N
  • Source:
    Insect science [Insect Sci] 2024 Aug; Vol. 31 (4), pp. 1296-1312. Date of Electronic Publication: 2023 Nov 15.
  • Publication Type:
    Journal Article
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Blackwell Pub Country of Publication: Australia NLM ID: 101266965 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1744-7917 (Electronic) Linking ISSN: 16729609 NLM ISO Abbreviation: Insect Sci Subsets: MEDLINE
    • Publication Information:
      Original Publication: Victoria, Australia : Blackwell Pub., c2005-
    • Subject Terms:
    • Abstract:
      Spodoptera frugiperda, also known as fall armyworm (FAW), is an invasive crop pest that can feed on a variety of host plants, posing a serious threat to food security. There are two sympatric strains of FAW that are morphologically identical but described with different food preferences: the "rice strain" (SfR) and the "corn strain" (SfC). A few genetic loci exist to identify these two strains. Mitochondrial and Z-chromosome-linked haplotypes are the most used, but the biggest part of the genome displays little polymorphism between strains that could explain their adaptation to different plants. We have previously observed consistent transcription differences between the strains in both laboratory and natural populations. Therefore, we wonder if there are effects from host-strain-associated loci, maternally or paternally inherited, on FAW performance that could explain the divergence between the two FAW strains. To test this hypothesis, we first produced two F 1 hybrid generations (SfR ♀ × SfC ♂, SfC ♀ × SfR ♂). These reciprocal hybrids should be heterozygous for all chromosomes except for the maternally inherited mitochondrial and sexual W chromosomes. To evaluate whether plant preference is determined by these genetic loci, we cultivated the two hybrids and the two parental strains in triplicate on an artificial diet and recorded several phenotypic traits such as weight over time, survival rate, emerging rate, developmental time, and sex ratio. Then, the same performance experiment was carried out on corn plants. Surprisingly, on the artificial diet, the two hybrid genotypes were both more performant than the two parental strains in terms of survival rate, pupal emerging rate, and developmental time, whereas they were intermediate to the inbred parental strains in pupal weight. On the corn plant diet, both hybrid genotypes outperformed the two parental strains in larval weight. Although these asymmetrical results revealed that mitochondrial or sex-linked haplotypes alone cannot explain the performance differences, they suggested a heterosis effect in FAW. A reduction of the female number for the CR genotype and the decreased F 1 offspring reproduction in both hybrids suggested the possibility of Haldane's rule, which might be explained by the dominance model.
      (© 2023 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.)
    • References:
      Allen, C.E., Zwaan, B.J. and Brakefield, P.M. (2011) Evolution of sexual dimorphism in the Lepidoptera. Annual Review of Entomology, 56, 445–464.
      Butt, B.A. and Cantu, E. (1962) Sex Determination of Lepidopterous Pupae. USDA‐ARS, Washington.
      Burton, R.S. and Barreto, F.S. (2012) A disproportionate role for mtDNA in Dobzhansky‐Muller incompatibilities? Molecular Biology, 21, 4942–4957.
      Burton, R.S., Pereira, R.J. and Barreto, F.S. (2013) Cytonuclear genomic interactions and hybrid breakdown. Annual Review of Ecology, Evolution, and Systematics, 44, 281–302.
      Bao, W.K. (1990) Opportunity and risk‐considerations for 40 years of breeding research. The Plant Journal, 4, 4–5.
      Baranwal, V.K., Mikkilineni, V., Zehr, U.B., Tyagi, A.K. and Kapoor, S. (2012) Heterosis: emerging ideas about hybrid vigour. Journal of Experimental Botany, 63, 6309–6314.
      Barratt, D.H.P. and Flavell, R.B. (1977) Mitochondrial complementation and grain yield in hybrid wheat. Annals of Botany, 41, 1333–1343.
      Beland, G.L. and Hatchett, J.H. (1976) Expression of antibiosis to the bollworm in two soybean genotypes. Journal of Economic Entomology, 69, 557–560.
      Bruce, A. (1910) The Mendelian theory of heredity and the augmentation of vigor. Science, 32, 627–628.
      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.
      Cañas‐Hoyos, N., Márquez, E.J. and Saldamando‐Benjumea, C.I. (2016) Heritability of wing size and shape of the rice and corn strains of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). Neotropical Entomology, 45, 411–419.
      Christie, J.S., Picornell, A., Moya, A., Ramon, M.M. and Castro, J.A. (2011) Mitochondrial DNA effects on fitness in Drosophila subobscura. Heredity, 107, 239–245.
      Combs, R.L. and Valério, J.R. (1980) Biology of the fall armyworm on four varieties of bermudagrass when held at constant temperatures. Environmental Entomology, 9, 393–396.
      Coyne, J. and Orr, H.A. (1989) Two rules of speciation. In Speciation and Its Consequences (eds. D. Otte & J. Endler), pp. 180–207. Sinauer Associates, Sunderland, MA, USA.
      Coyne, J.A. and Orr, H.A. (2004) Speciation. Sinauer Associates, Sunderland, MA.
      Davenport, C.B. (1908) Degeneration, albinism and inbreeding. Science, 28, 454–455.
      Das, S.K., Patnaik, S., Ghosh, B., Singh, T., Nair, B.P., Sen, S.K. et al. (1994) Heterosis analysis in some three‐way crosses of Bombyx mori L. Sericologia, 34, 51–61.
      Datta, R.K. (1984) Improvement of silkworm races (Bombyx mori L.) in India. Sericologia, 24, 393–415.
      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.
      Durand, K., Yainna, S. and Nam, K. (2022) Incipient speciation between host‐plant strains in the fall armyworm. BMC Ecology and Evolution, 22, 52.
      East, E.M. (1936) Heterosis. Genetics, 21, 375.
      Edmands, S. (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution; International Journal of Organic Evolution, 53, 1757–1768.
      Ekechukwu, N.E., Baeshen, R., Traorè, S.F., Coulibaly, M., Diabate, A., Catteruccia, F. et al. (2015) Heterosis increases fertility, fecundity, and survival of laboratory‐produced F1 hybrid males of the malaria mosquito Anopheles coluzzii. G3 Genes|Genomes|Genetics, 5, 2693–2709.
      Flint‐Garcia, S.A., Buckler, E.S., Tiffin, P., Ersoz, E. and Springer, N.M. (2009) Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS ONE, 4, e7433.
      Fisher, R.A. (1928) The possible modification of the response of the wild type to recurrent mutations. The American Naturalist, 62, 115–126.
      Fisher, R.A. (1930) Sexual reproduction and sexual selection. In The Genetical Theory of Natural Selection (ed. R.A. Fisher), p. 141. Oxford, UK: Clarendon Press.
      Fiteni, E., Durand, K., Gimenez, S., Meagher, R.L. Jr., 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.
      Gamo, T. (1976) On the recent concept and trends in silkworm breeding. Farming Japan, 10, 11–12.
      Giolo, F.P., Grutzmacher, A.D., Garcia, M.S. and Busato, G.R. (2002) Parâmetros biológicos de Spodoptera frugiperda (J. E. Smith, 1797) (Lep.: Noctuidae) oriundas de diferentes localidades e hospedeiros. Revista Brasileira De Agrociência, 8, 219–224.
      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.
      Ganiger, P.C., Yeshwanth, H.M., Muralimohan, K., Vinay, N., Kumar, A.R.V. and Chandrashekara, K. (2018) Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in the maize fields of Karnataka. Indian Current Science, 115, 621–623.
      Goergen, G., Kumar, P.L., Sankung, S.B., 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.
      Greaves, I.K., Groszmann, M., Ying, H., Taylor, J.M., Peacock, W.J. and Dennis, E.S. (2012) Trans chromosomal methylation in Arabidopsis hybrids. Proceedings of the National Academy of Sciences USA, 109, 3570–3575.
      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, 20.
      Groot, A.T., Marr, M., Heckel, D.G. and Schöfl, G. (2010) The roles and interactions of reproductive isolation mechanisms in fall armyworm (Lepidoptera: Noctuidae) host strains. Ecological Entomology, 35, 105–118.
      Groszmann, M., Greaves, I.K., Albertyn, Z.I., Scofield, G.N., Peacock, W.J. and Dennis, E.S. (2011) Changes in 24‐nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proceedings of the National Academy of Sciences USA, 108, 2617–2622.
      Grula, J.W. and Taylor, O.R. (1980) Some characteristics of hybrids derived from the sulfur butterflies, Colias eurytheme and C. philodice: phenotypic effects of X chromosome. Evolution; International Journal of Organic Evolution, 34, 673–687.
      Grunder, A. (1974) Mitochondrial heterosis. Poultry Science, 53, 1306–1314.
      Habib, M.E.M., Paleari, M.L. and Amaral, E.C. (1983) Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Lepidoptera: Noctuidae). Revista Brasileira De Zoologia, 1, 177–182.
      Haldane, J.B.S. (1922) Sex ratio and unisexual sterility in animal hybrids. Journal of Genetics, 12, 193–197.
      Harrison, R.G. (1993) Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford, United Kingdom.
      Howard, D.J. and Berlocher, S.H. (1998) Endless Forms: Species and Speciation. Oxford University Press, Oxford, United Kingdom.
      Howard, D.J., Reece, M., Gregory, P.G., Chu, J. and Cain, M.L. (1998) The evolution of barriers to fertilization between closely related organisms. In Endless Forms: Species and Speciation (eds. D.J. Howard & S.H. Berlocher), pp. 279–288. Oxford University Press, Oxford, United Kingdom.
      He, G., Zhu, X., Elling, A.A., Chen, L., Wang, X., Guo, L. et al. (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. The Plant Cell, 22, 17–33.
      Hoy, M.A. (1976) Genetic improvement of insects: fact or fantasy. Environmental Entomology, 5, 833–839.
      Jiggins, C.D. and Mallet, J. (2000) Bimodal hybrid zones and speciation. Trends in Ecology & Evolution, 15, 250–255.
      Jiggins, C.D., Naisbit, R.E., Coe, R.L. and Mallet, J. (2001) Reproductive isolation caused by color pattern mimicry. Nature, 411, 302–305.
      Johnson, S.J. (1987) Migration and the life history strategy of the fall armyworm, Spodoptera frugiperda in the western hemisphere. International Journal of Tropical Insect Science, 8, 543–549.
      Jones, D.F. (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics, 2, 466.
      Kaeppler, S. (2011) Heterosis: one boat at a time, or a rising tide? New Phytologist, 189, 900–902.
      Kaeppler, S. (2012) Heterosis: many genes, many mechanisms‐end the search for an undiscovered unifying theory. International Scholarly Research Notices, 2012, 682824.
      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.
      Kristensen, T.N. and Sorensen, A.C. (2005) Inbreeding—lessons from animal breeding, evolutionary biology and conservation genetics. Animal Science, 80, 121–133.
      Kost, S., Heckel, D.G., Yoshido, A., Marec, F. and Groot, A.T. (2016) A Z‐linked sterility locus causes sexual abstinence in hybrid females and facilitates speciation in Spodoptera frugiperda. Evolution; International Journal of Organic Evolution, 70, 1418–1427.
      Krishnaswamy, S. (1987) A new concept of a three‐way crosses in place of conventional Mysore × Bivoltine hybrids. Indian Silk, 27, 21–26.
      Lane, N. (2011) Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations. BioEssays, 33, 860–869.
      Li, X.J., Wu, M.F., Ma, J., Gao, B.Y., Wu, Q.L., Chen, A.D. et al. (2019) Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Management Science, 76, 454–463.
      Liao, X., Wei, M., Khan, A., Zhao, Y., Kong, X., Zhou, B. et al. (2020) Comparative analysis of mitochondrial genome and expression variation between UG93A and UG93B reveals a candidate gene related to cytoplasmic male sterility in kenaf. Industrial Crops and Products, 152, 112502.
      Lewter, J.A., Szalanski, A.L., Nagoshi, R.N., Meagher, R.L., Owens, C.B. and Luttrell, R.G. (2006) Genetic variation within and between strains of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomologist, 89, 63–68.
      Levy, H.C., Garcia‐Maruniak, A. and Maruniak, J.E. (2002) Strain identification of Spodoptera frugiperda (Lepidoptera: Noctuidae) insects and cell line: PCR‐RFLP of cytochrome oxidase subunit I gene. Florida Entomologist, 85, 186–190.
      Lu, Y.J. and Adang, M.J. (1996) Distinguishing fall armyworm (Lepidoptera: Noctuidae) strains using a diagnostic mitochondrial DNA marker. Florida Entomologist, 79, 48–55.
      Mather, K. and Jinks, J.L. (1971) Biometrical Genetics: the Study of Continuous Variation. Chapman and Hall, London.
      Machado, V., Wunder, M., Baldissera, V.D., Oliveira, J.V. and Fiu, L.M. (2008) Molecular characterization of host strains of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Southern Brazil. Annals of the Entomological Society of America, 101, 619–626.
      Martinelli, S., Barata, R.M., Zucchi, M.I., Silva‐Filho, M..C. and Omoto, C. (2006) Molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) populations associated to maize and cotton crops in Brazil. Journal of Economic Entomology, 99, 519–526.
      Meagher, R.L. and Gallo‐Meagher, M. (2003) Identifying host strains of fall armyworm (Lepidoptera: Noctuidae) in Florida using mitochondrial markers. Florida Entomologist, 86, 450–455.
      Meiklejohn, C.D., Holmbeck, M.A., Siddiq, M.A., Abt, D.N., Rand, D.M. and Montooth, K.L. (2013) An incompatibility between a mitochondrial tRNA and its nuclear‐encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genetics, 9, e1003238.
      Mitchell, E.R., McNeil, J.N., Westbrook, J.K., Silvain, J.F., Lalanne‐Cassou, B., Chalfant, R.B. et al. (1991) Seasonal periodicity of fall armyworm, (Lepidoptera: Noctuidae) in the Caribbean basin and northward to Canada. Journal of Entomological Science, 26, 39–50.
      Montezano, D.G., Specht, A., Sosa‐Gomez, 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.
      Machado, V.L.L., Giannotti, E. and Oliveira, R.M. (1985) Aspectos biológicos de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em couve. Anais Da Sociedade Entomológica Do Brasil, 14, 121–130.
      McDaniel, R.G. and Sarkissian, I.V. (1966) Heterosis: complementation by mitochondria. Science, 152, 1640–1642.
      McDaniel, R.G. and Grimwood, B.G. (1971) Hybrid vigor in Drosophila: respiration and mitochondrial energy conservation. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 38, 309–314.
      Montezano, D.G., Specht, A., Sosa‐Gómez, D.R., Roque‐Specht, V.F. and Barros, N.M. (2014) Immature stages of the armyworm, Spodoptera eridania: developmental parameters and host plants. Journal of Insect Science, 14, 238.
      Montezano, D.G., Specht, A., Sosa‐Gómez, D.R., Roque‐Specht, V.F., de Paula‐Moraes, S.V., Peterson, J.A. et al. (2019) Developmental parameters of Spodoptera frugiperda (Lepidoptera: Noctuidae) immature stages under controlled and standardized conditions. The Journal of Agricultural Science, 11, 76.
      Mukherjee, T.K., Stevens, R.W.C. and Hoogendoorn, M.P. (1970) Oxygen uptake of mitochondrial isolates from two breeds of chickens and their F1 cross. Poultry Science, 49, 1130–1131.
      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.
      Nagoshi, R.N., Meagher, R.L., Nuessly, G. and Hall, D.G. (2006) Effects of fall armyworm (Lepidoptera: Noctuidae) interstrain mating in wild populations. Environmental Entomology, 35, 561–568.
      Nagoshi, R.N., Meagher, R.L., Adamczyk, J.J., Braman, S.K., Brandenburg, R.L. and Nuessly, G. (2006) New restriction fragment length polymorphisms in the cytochrome oxidase I gene facilitate host strain identification of fall armyworm (Lepidoptera: Noctuidae) populations in the southeastern United States. Journal of Economic Entomology, 99, 671–677.
      Nagoshi, R.N. (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.
      Nagoshi, R.N. (2019) Evidence that a major subpopulation of fall armyworm found in the Western Hemisphere is rare or absent in Africa, which may limit the range of crops at risk of infestation. PLoS ONE, 14, e0208966.
      Nagoshi, R.N., Goergen, G., Koffi, D., Agboka, K., Adjevi, A.K.M., Plessis, H.D. 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.
      Nagoshi, R.N. and Meagher, R. (2003) Fall armyworm FR sequences map to sex chromosomes and their distribution in the wild indicate limitations in interstrain mating. Insect Molecular Biology, 12, 453–458.
      Ni, Z., Kim, E.D., Ha, M., Lackey, E., Liu, J., Zhang, Y. et al. (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature, 457, 327–331.
      Nosil, P. (2012) Ecological Speciation. Oxford University Press, Oxford, United Kingdom.
      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.
      Pashley, D.P., Johnson, S.J. and Sparks, A.N. (1985) Genetic population structure of migratory moths: the fall armyworm (Lepidoptera, Noctuidae). Annals of the Entomological Society of America, 78, 756–762.
      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.
      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.
      Pashley, D.P. (1988) Quantitative genetics, development, and physiological adaptation in host strains of fall armyworm. Evolution; International Journal of Organic Evolution, 42, 93–102.
      Pashley, D.P. (1989) Host‐associated differentiation in armyworms (Lepidoptera: Noctuidae): an allozymicand mitochondrial DNA perspective. In Electrophoretic Studies on Agricultural Pests (eds. H.D. Loxdale & J. der Hollander), pp. 103–114. Oxford University Press, Oxford, United Kingdom.
      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.
      Poitout, S., Bues, R. and Rumeur, C.L. (1972) Élevage sur milieu artificiel simple de deux Noctuelles parasites du coton Earias insulana et Spodoptera littoralis. Entomologia Experimentalis et Applicata, 15, 341–350.
      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.
      Prowell, D.P. (1998) Sex linkage and speciation in Lepidoptera. In Endless Forms: Species and Speciation (eds. D.J. Howard & S.H. Berlocher), pp. 309–319. Oxford University Press, Oxford, United Kingdom.
      Pantoja, A., Smith, C.M. and Robinson, J.F. (1987) Development of the fall armyworm, Spodoptera frugiperda, strains from Louisiana and Puerto Rico. Environmental Entomology, 16, 116–119.
      Parra, J.R.P. and Carvalho, S.M. (1984) Biologia e nutrição quantitativa de Spodoptera frugiperda (J. E. Smith, 1797) em meios artificiais compostos de diferentes variedades de feijão. Anais Da Sociedade Entomológica Do Brasil, 13, 306–319.
      Presgraves, D.C. (2002) Patterns of postzygotic isolation in Lepidoptera. Evolution; International Journal of Organic Evolution, 56, 1168–1183.
      Pierron, D., Wildman, D.E., Hüttemann, M., Markondapatnaikuni, G.C., Aras, S. and Grossman, L.I. (2012) Cytochrome c oxidase: evolution of control via nuclear subunit addition. Biochimica Et Biophysica Acta. Bioenergetics, 1817, 590–597.
      R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R‐project.org/.
      Rand, D.M., Fry, A. and Sheldahl, L. (2006) Nuclear–mitochondrial epistasis and drosophila aging: introgression of Drosophila simulans mtDNA modifies longevity in D. melanogaster nuclear backgrounds. Genetics, 172, 329–341.
      Richie, M.G. and Phillips, S.D.F. (1998) The genetics of sexual isolation. In Endless Forms: Species and Speciation (eds. D.J. Howard & S.H. Berlocher), pp. 291–308. Oxford University Press, Oxford, United Kingdom.
      Ritchie, S.W., Hanway, J.J. and Benson, G.O. (1992) How a Corn Plant Develops. Iowa State University of Science and Technology, Cooperative Extension Service, Ames, Iowa.
      Rockey, S.J., Hainze, J.H. and Scriber, J.M. (1987) Evidence of sex linked diapause response in Papilio glaucus subspecies and their hybrids. Physiological Entomology, 12, 181–184.
      Rogers, C.E. and Marti, O.G. (1994) Reproductive potential of once‐mated moths of the fall armyworm (Lepidoptera: Noctuidae). Florida Entomologist, 77, 402–410.
      Rogers, C.E. and Marti, O.G. (1997) Once‐mated beet armyworm (Lepidoptera: Noctuidae): effects of age at mating on fecundity, fertility, and longevity. Environmental Entomology, 26, 585–590.
      Srivastava, H.K. and Sarkissian, I.V. (1972) Mitochondrial polymorphism. IV. Phospholipid composition of mitochondria of a wheat hybrid and its parents. Biochemical Genetics, 7, 347–354.
      Schlum, K.A., Lamour, K., de Bortoli, C.P., Banerjee, R., Meagher, R., Pereira, E. et al. (2021) Whole genome comparisons reveal panmixia among fall armyworm (Spodoptera frugiperda) from diverse locations. BMC Genomics [Electronic Resource], 22, 179.
      Shen, H., He, H., Li, J., Chen, W., Wang, X., Guo, L. et al. (2012) Genome‐wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. The Plant Cell, 24, 875–892.
      Specht, A., Montezano, D.G., Sosa‐Gómez, D.R., Paula‐Moraes, S.V., Roque‐Specht, V.F. and Barros, N.M. (2016) Reproductive potential of Spodoptera eridania (Stoll) (Lepidoptera: Noctuidae) in the laboratory: effect of multiple couples and the size. Brazilian Journal of Biology, 76, 526–530.
      Sperling, F.A.H. (1994) Sex‐linked genes and species differences in Lepidoptera. The Canadian Entomologist, 126, 807–818.
      Specht, A. and Roque‐Specht, V.F. (2016) Immature stages of Spodoptera cosmioides (Lepidoptera: Noctuidae): developmental parameters and host plants. Revista Zoologia, 33, e20160053.
      Sheridan, A. (1981) Cross breeding and heterosis animal breeding. Animal Breeding Abstracts, 49, 131–144.
      Shull, G.H. (1908) The composition of a field of maize. Journal of Heredity, 4, 296–301.
      Stupar, R.M. and Springer, N.M. (2006) cis‐transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics, 173, 2199–2210.
      Swanson‐Wagner, R.A., Jia, Y., DeCook, R., Borsuk, L.A., Nettleton, D. and Schnable, P.S. (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proceedings of the National Academy of Sciences USA, 103, 6805–6810.
      Swanson‐Wagner, R.A., Decook, R., Jia, Y., Bancroft, T., Ji, T., Zhao, X.F. et al. (2009) Paternal dominance of trans‐eQTL influences gene expression patterns in maize hybrids. Science, 326, 1118–1120.
      Silva‐Brandão, K.L., Horikoshi, R.J., Bernardi, D., Omoto, C., Figueira, A. and Brandão, M.M. (2017) Transcript expression plasticity as a response to alternative larval host plants in the speciation process of corn and rice strains of Spodoptera frugiperda. BMC Genomics [Electronic Resource], 18, 792.
      Tisdale, R.A. and Sappington, T.W. (2001) Realized and potential fecundity, egg fertility, and longevity of laboratory‐reared female beet armyworm (Lepidoptera: Noctuidae) under different adult diet regimes. Annals of the Entomological Society of America, 94, 415–419.
      Turelli, M. and Moyle, L.C. (2007) Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics, 176, 1059–1088.
      Vakifahmetoglu‐Norberg, H., Ouchida, A.T. and Norberg, E. (2017) The role of mitochondria in metabolism and cell death. Biochemical and Biophysical Research Communications, 482, 426–431.
      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.
      Virmani, S.S. (1994) Heterosis and Hybrid Rice Breeding. Springer, Berlin, Germany, and International Rice Research Institute, Manila, Philippines.
      Westbrook, J.K., Nagoshi, R.N., Meagher, R.L., Fleischer, S.J. and Jairam, S. (2016) Modeling seasonal migration of fall armyworm moths. International Journal of Biometeorology, 60, 255–267.
      Whitford, F., Quisenberry, S.S., Riley, T.J. and Lee, J.W. (1988) Oviposition preference, mating compatibility, and development of two fall armyworm strains. Florida Entomologist, 71, 234–243.
      Xue, M., Pang, Y.H., Wang, H.T., Li, Q.L. and Liu, T.X. (2010) Effects of four plants on biology and food utilization of the cutworm, Spodoptera litura. Journal of Insect Science, 10, 22.
      Yainna, S., Tay, W.T., Fiteni, E., Legeai, F., Clamens, A.L., Gimenez, S. et al. (2020) Genomic balancing selection is key to the invasive success of the fall armyworm. Authorea, https://doi.org/10.22541/au.160363803.32074105/v1.
      Yao, H., Gray, A.D., Auger, D.L. and Birchler, J.A. (2013) Genomic dosage effects on heterosis in triploid maize. Proceedings of the National Academy of Sciences USA, 110, 2665–2669.
      Yu, D., Gu, X., Zhang, S., Dong, S., Miao, H., Gebretsadik, K. et al. (2021) Molecular basis of heterosis and related breeding strategies reveal its importance in vegetable breeding. Horticulture Research, 8, 120.
      Zhang, L., Liu, B., Jiang, Y., Liu, J., Wu, K. and Xiao, Y. (2019) Molecular characterization analysis of fall armyworm populations in China. Plant Protection, 45, 10–27.
      Zhang, L., Liu, B., Zheng, W.G., Liu, C.H., Zhang, D.D., Zhao, S.Y. et al. (2020) Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Molecular Ecology Resources, 20, 1682–1696.
    • Grant Information:
      202008440426 China Scholarship Council
    • Contributed Indexing:
      Keywords: Haldane's rule; fall armyworm; heterosis; hybrid performance; mitochondria
    • Publication Date:
      Date Created: 20231116 Date Completed: 20240813 Latest Revision: 20240813
    • Publication Date:
      20240813
    • Accession Number:
      10.1111/1744-7917.13295
    • Accession Number:
      37969057