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Changes in the genetic composition of Myzus persicae nicotianae populations in Chile and frequency of insecticide resistance mutations

Published online by Cambridge University Press:  07 October 2021

Marco A. Cabrera-Brandt Open the ORCID record for Marco A. Cabrera-Brandt [Opens in a new window] ,
Amalia Kati ,
María E. Rubio-Meléndez ,
Christian C. Figueroa  and
Eduardo Fuentes-Contreras
Marco A. Cabrera-Brandt*
Affiliation:
Facultad de Ciencias Agrarias, Centre for Molecular and Functional Ecology in Agroecosystems, Universidad de Talca, Casilla 747, Talca, Chile
Amalia Kati
Affiliation:
Plant Pathology Laboratory, School of Agriculture, Aristotle University of Thessaloniki, Thessaloniki, Greece
María E. Rubio-Meléndez
Affiliation:
Facultad de Ingeniería, Centre for Bioinformatics and Molecular Simulation, Universidad de Talca, Casilla 747, Talca, Chile
Christian C. Figueroa
Affiliation:
Centre for Molecular and Functional Ecology in Agroecosystems, Instituto de Ciencias Biológicas, Universidad de Talca, Casilla 747, Talca, Chile
Eduardo Fuentes-Contreras
Affiliation:
Facultad de Ciencias Agrarias, Centre for Molecular and Functional Ecology in Agroecosystems, Universidad de Talca, Casilla 747, Talca, Chile
*
Author for correspondence: Marco A. Cabrera-Brandt, Email: [email protected]
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Abstract

Myzus persicae is a cosmopolitan aphid that is highly polyphagous and an important agricultural pest. The subspecies M. persicae nicotianae has been described for highly specialized phenotypes adapted to tobacco (Nicotiana tabacum). In Chile, the population of M. persicae nicotianae was originally composed of a single red genotype that did not possess insecticide resistance mutations. However, in the last decade, variation in the colour of tobacco aphids has been observed in the field. To determine whether this variation stems from the presence of new genotypes, sampling was carried out across the entire distribution of tobacco cultivation regions in Chile. The aphids collected were genotyped, and the frequency of kdr (L1014F), super-kdr (M918T), modification of acetylcholinesterase (MACE) and nicotinic acetylcholine receptor β subunit (nAChRβ) mutations associated with insecticide resistance was determined. A total of 16 new genotypes of M. persicae nicotianae were detected in Chile: four of them possessed the MACE mutation, and none of them possessed the kdr, super-kdr or nAChRβ mutation. The previously described red genotype was not detected in any of the sampled fields over two seasons. These results raise questions about the mechanisms underlying changes in the genetic structure of M. persicae nicotianae populations in Chile. Future research aimed at addressing these questions could provide new insight into aphid evolution and agricultural practices.

Keywords

Clonal diversitymutational insecticide resistanceMyzus persicae nicotianae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 6 , December 2021 , pp. 759 - 767
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Anstead, JA, Williamson, MS, Eleftherianos, L and Denholm, I (2004) High-throughput detection of knockdown resistance in Myzus persicae using allelic discriminating quantitative PCR. Insect Biochemistry and Molecular Biology 34, 871–877.CrossRefGoogle ScholarPubMed
Anstead, JA, Williamson, MS and Denholm, I (2008) New methods for the detection of insecticide resistant Myzus persicae in U.K. suction trap network. Agricultural and Forest Entomology 10, 291–295.CrossRefGoogle Scholar
Arnaud-Haond, S and Belkhir, K (2007). GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes 7, 15–17.CrossRefGoogle Scholar
Bass, C, Puinean, AM, Andrews, MC, Culter, P, Daniels, M, Elias, J, Laura Paul, V, Crossthwaite, AJ, Denholm, I, Field, LM, Foster, SP, Lind, R, Williamson, MS and Slater, R (2011) Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neuroscience 12, 51.CrossRefGoogle ScholarPubMed
Bass, C, Zimmer, CT, Riveron, JM, Wilding, CS, Wondji, CS, Kaussmann, M, Field, LM, Williamson, MS and Nauen, R (2013). Gene amplification and microsatellite polymorphism underlie a recent insect host shift. Proceedings of the National Academy of Sciences of the USA 110, 19460–19465.CrossRefGoogle ScholarPubMed
Bass, C, Puinean, AM, Zimmer, CT, Denholm, I, Field, LM, Foster, SP, Gutbrod, O, Nauen, R, Slater, R and Williamson, MS (2014). The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology 51, 41–51.CrossRefGoogle ScholarPubMed
Bebber, DP (2015) Range-expanding pests and pathogens in a warming world. Annual Review of Phytopathology 53, 335–356.CrossRefGoogle Scholar
Bell, JR, Alderson, L, Izera, D, Kruger, T, Parker, S, Pickup, J, Shortall, CR, Taylor, MS, Verrier, P and Harrington, R (2015). Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. Journal of Animal Ecology 84, 21–34.CrossRefGoogle ScholarPubMed
Blackman, RL and Eastop, VF (2000). Aphids on the World's Crops: An Identification and Information Guide. 2nd Edn. Chichester, England: Wiley, p. 476.Google Scholar
Blackman, RL and Eastop, VF (2017) Taxonomic issues. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests. Wallingford, UK: CAB International, pp. 1–36.Google Scholar
Blackman, RL, Malarky, G, Margaritopoulos, JT and Tsitsipis, JA (2007). Distribution of common genotypes of Myzus persicae (Hemiptera: Aphididae) in Greece, in relation to life cycle and host plant. Bulletin of Entomological Research 97, 253–263.CrossRefGoogle ScholarPubMed
Cabrera-Brandt, MA, Fuentes-Contreras, E and Figueroa, CC (2010) Differences in the detoxification metabolism between two clonal lineages of the aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) reared on tobacco (Nicotiana tabacum L.). Chilean Journal of Agricultural Research 70, 567–575.CrossRefGoogle Scholar
Cabrera-Brandt, MA, Silva, AX, Le Trionnaire, G, Tagu, D and Figueroa, CC (2014) Transcriptomic responses of the aphid Myzus persicae nicotianae Blackman (Hemiptera: Aphididae) to insecticides: analyses in the single Chilean clone of the tobacco aphid. Chilean Journal of Agricultural Research 74, 191–199.CrossRefGoogle Scholar
Cabrera-Brandt, MA, Verdugo, JA, Ramírez, CC, Lacroze, JP, Sauge, MH and Figueroa, CC (2015) Intra-specific variation of behavioral signals in suppressing plant defenses in the green peach aphid Myzus persicae, feeding on the resistant wild peach Prunus davidiana. Journal of Pest Science 88, 259–266.CrossRefGoogle Scholar
Clements, KM, Sorenson, CE, Wiegmann, BM, Neese, PA and Roe, RM (2000 a) Genetic, biochemical, and behavioral uniformity among populations of Myzus nicotianae and Myzus persicae. Entomologia Experimentalis et Applicata 95, 269–281.CrossRefGoogle Scholar
Clements, KM, Wiegmann, BM, Sorenson, CE, Smith, CF, Neese, PA and Roe, RM (2000 b) Genetic variation in the Myzus persicae complex (Homoptera: Aphididae): evidence for a single species. Annals of the Entomological Society of America 93, 31–46.CrossRefGoogle Scholar
Earl, DA and von Holdt, BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 59–361.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
Excoffier, L, Smouse, PE and Quattro, JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
Figueroa, CC, Fuentes-Contreras, E, Molina-Montenegro, MA and Ramírez, CC (2018) Biological and genetic features of introduced aphid populations in agroecosystems. Current Opinion in Insect Science 26, 63–68.CrossRefGoogle ScholarPubMed
Fontaine, S, Caddoux, L, Brazier, C, Bertho, C, Bertolla, P, Micoud, A and Roy, L (2011). Uncommon associations in target resistance among French populations of Myzus persicae from oilseed rape crops. Pest Management Science 67, 881–885.CrossRefGoogle ScholarPubMed
Foster, SP, Devine, G and Devonshire, AL (2017) Insecticide resistance. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests. Wallingford, UK: CAB International, pp. 426–447.CrossRefGoogle Scholar
Fuentes-Contreras, E, Figueroa, CC, Reyes, M, Briones, LM and Niemeyer, HN (2004) Genetic diversity and insecticide resistance of Myzus persicae (Hemiptera: Aphididae) populations from tobacco in Chile: evidence for the existence of a single predominant clone. Bulletin of Entomological Research 94, 11–18.CrossRefGoogle ScholarPubMed
Fuentes-Contreras, E, Basoalto, E, Sandoval, C, Pavez, P, Leal, C, Burgos, R and Muñoz, C (2007) Evaluación de la eficacia, efecto residual y de volteo de aplicaciones en pretrasplante de insecticidas nicotinoides y mezclas de nicotinoide-piretroide para el control de Myzus persicae nicotianae (Hemiptera: Aphididae) en tabaco. Agricultura Técnica (Chile) 67, 16–22.Google Scholar
Harlow, CD and Lampert, EP (1990). Resistance mechanisms in two color forms of the tobacco aphid (Homoptera: Aphididae). Journal of Economic Entomology 83, 2130–2135.CrossRefGoogle Scholar
Kati, AN, Mandrioli, M, Skouras, PJ, Malloch, GL, Voudouris, CC, Venturelli, M, Manicardi, GC, Tsitsipis, JA, Fenton, B and Margaritopoulos, JT (2014) Recent changes in the distribution of carboxylesterase genes and associated chromosomal rearrangements in Greek populations of the tobacco aphid Myzus persicae nicotianae. Biological Journal of the Linnean Society 113, 455–470.CrossRefGoogle Scholar
Margaritopoulos, JT, Tsitsipis, JA, Zintzaras, E and Blackman, RL (2000) Host-correlated morphological variation of Myzus persicae (Sulzer) (Homoptera: Aphididae) populations in Greece. Bulletin of Entomological Research 90, 233–244.CrossRefGoogle Scholar
Margaritopoulos, JT, Tsitsipis, JA, Goundoudaki, S and Blackman, RL (2002) Life cycle variation of Myzus persicae (Sulzer) (Hemiptera: Aphididae) in Greece. Bulletin of Entomological Research 92, 309–320.CrossRefGoogle Scholar
Margaritopoulos, JT, Blackman, RL, Tsitsipis, JA and Sannino, L (2003) Coexistence of different host-adapted forms of the Myzus persicae group (Hemiptera: Aphididae) in southern Italy. Bulletin of Entomological Research 93, 131–135.CrossRefGoogle Scholar
Margaritopoulos, JT, Malarky, G, Tsitsipis, JA and Blackman, RL (2007 a) Microsatellite DNA and behavioural studies provide evidence of host-mediated speciation in Myzus persicae (Hemiptera: Aphididae). Biological Journal of the Linnean Society 91, 687–902.CrossRefGoogle Scholar
Margaritopoulos, JT, Skouras, PJ, Nikolaidou, P, Manolikaki, J, Maritsa, K, Tsamandani, K, Kanavaki, OM, Bacandritsos, N, Zarpas, KD and Tsitsipis, JA (2007 b) Insecticide resistance status of Myzus persicae (Hemiptera: Aphididae) populations from peach and tobacco in mainland Greece. Pest Management Science 63, 821–829.CrossRefGoogle ScholarPubMed
Margaritopoulos, JT, Kati, AN, Voudouris, CC, Skouras, PJ and Tsitsipis, JA (2021) Long-term studies on the evolution of resistance of Myzus persicae (Hemiptera: Aphididae) to insecticides in Greece. Bulletin of Entomological Research 111, 1–16.CrossRefGoogle Scholar
Mingeot, D, Hautier, L and Jansen, JP (2021). Structuration of multilocus genotypes associated with insecticide resistance of the peach potato aphid, Myzus persicae (Sulzer), in potato fields in southern Belgium. Pest Management Science 77, 482–491.CrossRefGoogle Scholar
Nibouche, S, Fartek, B, Mississipi, S, Delatte, H, Reynaud, B and Costet, L (2014) Low genetic diversity in Melanaphis sacchari aphid populations at the worldwide scale. PLoS One 9, e106067.CrossRefGoogle Scholar
Nikolakakis, NN, Margaritopoulos, JT and Tsitsipis, JA (2003) Performance of Myzus persicae (Hemiptera: Aphididae) clones on different host-plants and their host preference. Bulletin of Entomological Research 93, 235–242.CrossRefGoogle ScholarPubMed
Olivares-Donoso, R, Troncoso, AJ, Tapia, DH, Aguilera-Olivares, D and Niemeyer, HM (2007). Contrasting performances of generalist and specialist Myzus persicae (Hemiptera: Aphididae) reveal differential prevalence of maternal effects after host transfer. Bulletin of Entomological Research 97, 61–67.CrossRefGoogle ScholarPubMed
Pan, Y, Peng, T, Xu, P, Zeng, X, Tian, F, Song, J and Shang, Q (2019 a) Transcription factors AhR/ARNT regulate the expression of CYP6CY3 and CYP6CY4 switch conferring nicotine adaptation. International Journal of Molecular Sciences 20, 4521.CrossRefGoogle ScholarPubMed
Pan, Y, Xu, P, Zeng, X, Liu, X and Shang, Q (2019 b) Characterization of UDP-glucuronosyltransferases and the potential contribution to nicotine tolerance in Myzus persicae. International Journal of Molecular Sciences 20, 3637.CrossRefGoogle ScholarPubMed
Panini, M, Dradi, D, Marani, G, Butturini, A and Mazzoni, E (2014). Detecting the presence of target-site resistance to neonicotinoids and pyrethroids in Italian populations of Myzus persicae. Pest Management Science 70, 931–938.CrossRefGoogle ScholarPubMed
Peakall, R and Smouse, PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.CrossRefGoogle Scholar
Peakall, R, Smouse, PE and Huff, DR (1995) Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss (Buchloë dactyloides (Nutt.) Engelm.). Molecular Ecology 4, 135–147.CrossRefGoogle Scholar
Peng, T, Pan, Y, Gao, X, Xi, J, Zhang, L, Ma, K, Wu, Y, Zhang, J and Shang, Q (2016). Reduced abundance of the CYP6CY3-targeting let-7 and miR-100 miRNAs accounts for host adaptation of Myzus persicae nicotianae. Insect Biochemistry and Molecular Biology 75, 89–97.CrossRefGoogle ScholarPubMed
Poupoulidou, D, Margaritopoulos, JT, Kephalogianni, TE, Zarpas, KD and Tsitsipis, JA (2006) Effect of temperature and photoperiod on the life cycle in lineages of Myzus persicae nicotianae and Myzus persicae s. str. (Hemiptera: Aphididae). European Journal of Entomology 103, 337–346.CrossRefGoogle Scholar
Pritchard, JK, Stephens, M and Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.CrossRefGoogle ScholarPubMed
Puinean, AM, Foster, SP, Oliphant, L, Denholm, I, Field, LM, Millar, NS, Williamson, MS and Bass, C (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genetics 6, e1000999.CrossRefGoogle ScholarPubMed
Raymond, M and Rousset, F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Rubiano-Rodríguez, JA, Fuentes-Contreras, E, Figueroa, CC, Margaritopoulos, JT, Briones, LM and Ramírez, CC (2014) Genetic diversity and insecticide resistance during the growing season in the green peach aphid (Hemiptera: Aphididae) on primary and secondary hosts: a farm-scale study in central. Bulletin of Entomological Research 104, 182–194.CrossRefGoogle ScholarPubMed
Rubiano-Rodríguez, JA, Fuentes-Contreras, E and Ramírez, C (2019). Variabilidad genética neutral y presencia de mecanismos de resistencia en Myzus persicae (Hemiptera: Aphididae), provenientes de diferentes hospedantes en Chile central. Ciencia y Tecnología Agropecuaria 20, 611–633.CrossRefGoogle Scholar
Rubio-Meléndez, ME, Sepúlveda, DA and Ramírez, CC (2018) Temporal and spatial distribution of insecticide resistance mutations in the green peach aphid Myzus persicae (Hemiptera: Aphididae) on primary and secondary host plants in central Chile. Pest Management Science 74, 340–347.CrossRefGoogle ScholarPubMed
Schuelke, M (2000) An economic method for the fluorescent labelling of PCR fragments. Nature Biotechnology 18, 233–234.CrossRefGoogle Scholar
Shigehara, T and Takada, H (2003) Changes in genotypic composition of Myzus persicae (Hemiptera: Aphididae) on tobacco during the past two decades in Japan. Bulletin of Entomological Research 93, 537–544.CrossRefGoogle ScholarPubMed
Shigehara, T and Takada, H (2004) Mode of inheritance of the polymorphic esterases in Myzus persicae (Hemiptera: Aphididae) in Japan. Bulletin of Entomological Research 94, 65–74.CrossRefGoogle ScholarPubMed
Singh, KS, Troczka, BJ, Duarte, A, Balabanidou, V, Trissi, N, Paladino, LZC, Nguyen, P, Zimmer, CT, Papapostolou, KM, Randall, E, Luke, B, Marec, F, Mazzoni, E, Williamson, MS, Hayward, A, Nauen, R, Vontas, J and Bass, C (2020) The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses. Science Advances 6, eaba1070.CrossRefGoogle ScholarPubMed
Srigiriraju, L, Semtner, PJ, Anderson, TD and Bloomquist, JR (2009) Esterase-based resistance in the tobacco-adapted form of the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in the Eastern United States. Archives of Insect Biochemistry and Physiology 72, 105–123.CrossRefGoogle Scholar
Tapia, DH, Troncoso, AJ, Vargas, RR, Olivares-Donoso, R and Niemeyer, HM (2008) Experimental evidence for competitive exclusion of Myzus persicae nicotianae by Myzus persicae s.s. (Hemiptera: Aphididae) on sweet pepper, Capsicum annuum (Solanaceae). European Journal of Entomology 105, 643–648.CrossRefGoogle Scholar
Tapia, DH, Silva, AX, Ballesteros, GI, Figueroa, CC, Niemeyer, HM and Ramírez, CC (2015) Differences in learning and memory of host plant features between specialist and generalist phytophagous insects. Animal Behaviour 106, 1–10.CrossRefGoogle Scholar
Troncoso, AJ, Vargas, RR, Tapia, DH, Olivares-Donoso, R and Niemeyer, HM (2005) Host selection by the generalist aphid Myzus persicae (Hemiptera: Aphididae) and its subspecies specialized on tobacco, after being reared on the same host. Bulletin of Entomological Research 95, 23–28.CrossRefGoogle ScholarPubMed
Turcotte, MM, Reznick, DN and Hare, JD (2011) The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics. Ecology Letters 14, 1084–1092.CrossRefGoogle ScholarPubMed
Vargas, RR, Troncoso, AJ, Tapia, DH, Olivares-Donoso, R and Niemeyer, HM (2005) Behavioural differences during host selection between alate virginoparae of generalist and tobacco-specialist Myzus persicae. Entomologia Experimentalis et Applicata 116, 43–53.CrossRefGoogle Scholar
Vorburger, C, Lancaster, M and Sunnucks, P (2003) Environmentally related patterns of reproductive modes in the aphid Myzus persicae, and the predominance of two ‘superclones’ in Victoria Australia. Molecular Ecology 12, 3493–3504.CrossRefGoogle ScholarPubMed
Voudouris, CC, Kati, AN, Sadikoglou, E, Williamson, M, Skouras, PJ, Dimotsiou, O, Georgiou, S, Fenton, B, Skavdis, G and Margaritopoulos, JT (2016) Insecticide resistance status of Myzus persicae in Greece: long-term surveys and new diagnostics for resistance mechanisms. Pest Management Science 72, 671–683.CrossRefGoogle ScholarPubMed
Voudouris, CC, Williamson, MS, Skouras, PJ, Kati, AN, Sahinoglou, AJ and Margaritopoulos, JT (2017) Evolution of imidacloprid resistance in Myzus persicae in Greece and susceptibility data for spirotetramat. Pest Management Science 73, 1804–1812.CrossRefGoogle ScholarPubMed
Vučetić, A, Petrović-Obradović, O and Stanisavljević, LŽ (2010) Morphological variation of Myzus persicae (Hemiptera: Aphididae) from peach and tobacco in Serbia and Montenegro. Archives of Biological Sciences 62, 767–774.CrossRefGoogle Scholar
Zepeda-Paulo, FA, Simon, JC, Ramírez, CC, Fuentes-Contreras, E, Margaritopoulos, JT, Wilson, AC, Sorenson, CE, Briones, LM, Azevedo, R, Ohashi, DV, Lacroix, C, Glais, L and Figueroa, CC (2010) The invasion route for an insect pest species: the tobacco aphid in the New World. Molecular Ecology 19, 4738–4752.CrossRefGoogle ScholarPubMed
Zitoudi, K, Margaritopoulos, JT, Mamuris, Z and Tsitsipis, JA (2001) Genetic variation in Myzus persicae populations associated with host-plant and life cycle category. Entomologia Experimentalis et Applicata 99, 303–311.CrossRefGoogle Scholar