Drosophila suzukii (Diptera: Drosophilidae) is a highly polyphagous fruit pest native to eastern Asia, which in the last decade had widely expanded its range and become a serious pest in the Americas and Europe. Invasion routes and the genetic diversity in populations of South America are poorly studied. Here, we compared the patterns of genetic variation of native populations and previously invaded regions (in America and Europe) with the genetic diversity of the recent invasion in Argentina. In addition, we explored the regional trade routes and volume of host fruits (Argentina, Brazil, Chile and Uruguay) to understand propagule pressure. We report for the first time a genetic assessment of the invasion history of D. suzukii in Argentina, noting genetic diversity at Cytochrome c oxidase subunit I gene fragment comparable with other recently colonized countries. In the years prior to the invasion into South America, Brazil imported large quantities of potential host fruits from different countries that had been previously invaded; likely Brazil might be the main source of D. suzukii in Argentina. This is emphasized by the fact that Argentina and Brazil share haplotypes; however, direct commercial pathway with the USA cannot be discarded, and additional sources of species arrivals are also possible. Our results suggest at least two invasion events could have occurred in Argentina, originating both from previously invaded areas (i.e., North America and Brazil). Our study provides information to improve our understanding of the routes and factors affecting the invasion of this economically significant pest in South America.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Individual COI sequences of SWD Argentina samples were deposited to GenBank (https://www.ncbi.nlm.nih.gov/). Accession numbers MH795917-MH795938.
(SAG) Servicio Agrícola y Ganadero (2017) Medidas Fitosanitarias de Emergencia provisionales para la plaga drosófila de las alas manchadas—Drosophila suzukii (Matsumura) Diptera: drosophilidae. Resolución Exenta No.:3672/2017
Adrion JR, Kousathanas A, Pascual M et al (2014) Drosophila suzukii: the genetic footprint of a recent, worldwide invasion. Mol Biol Evol 31(12):3148–3163. https://doi.org/10.1093/molbev/msu246
Anderson PK, Cunningham AA, Patel NG et al (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19(10):535–544. https://doi.org/10.1016/j.tree.2004.07.021
Ascunce MS, Yang CC, Oakey J et al (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331(6020):1066–1068. https://doi.org/10.1126/science.1198734
Asplen MK, Anfora G, Biondi A et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88(3):469–494. https://doi.org/10.1007/s10340-015-0681-z
Aukema JE, McCullough DG, Von Holle B et al (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60(11):886–897. https://doi.org/10.1525/bio.2010.60.11.5
Bebber DP, Ramotowski MAT, Gurr SJ (2013) Crop pests and pathogens move polewards in a warming world. Nat Clim Change 3(11):985–988. https://doi.org/10.1038/nclimate1990
Bellamy DE, Sisterson MS, Walse SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS One 8(4):e61227
Bolda MP, Goodhue RE, Zalom FG (2010) Spotted wing drosophila: potential economic impact of newly established pest. Giannini Foundation of Agricultural Economics, University of California. Agric Resour Econ Update 13(3):5–8
Carvajal JI (2010) Genetic diversity of Drosophila suzukii in San Diego. Dros Inf Serv 93(12):223–303. https://doi.org/10.1016/j.cub.2012.11.021
Chia-Hua L, Mottern JL, Walsh GC (2017) New record for the invasive spotted wing drosophila, Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) in Anillaco, western Argentina. Proc Entomol Soc Wash 119(1):146–150. https://doi.org/10.4289/0013-87188.8.131.52
Choi D, Park JS, Kim MJ et al (2017) Geographic variation in the spotted-wing drosophila, Drosophila suzukii (Diptera: Drosophilidae), based on mitochondrial DNA sequences. Mitochondrial DNA Part A. https://doi.org/10.1080/24701394.2016.1278534
Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. B Insectol 65(1):149–160
Cini A, Anfora LA, Escudero-Colomar A, Grassi A et al (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J Pest Sci 87:559–566
Ciosi M, Miller NJ, Kim KS et al (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627. https://doi.org/10.1111/j.1365-294X.2008.03866.x
de la Vega GJ, Corley JC (2019) Drosophila suzukii (Diptera: Drosophilidae) distribution modelling improves our understanding of pest range limits. J. Pest Manage, Int. https://doi.org/10.1080/09670874.2018.1547460
De Ros G, Conci S, Pantezzi T, Savini G (2015) The economic impact of invasive pest Drosophila suzukii on berry production in the Province of Trento. Italy. J Berry Res 5(2):89–96
Deprá M, Poppe JL, Schmitz HJ, De Toni DC, Valente VLS (2014) The first records of the invasive pest Drosophila suzukii in the South American continent. J Pest Sci 87(3):379–383
Desvars-Larrive A, Hammed A, Hodroge A et al (2018) Population genetics and genotyping as tools for planning rat management programmes. J Pest Sci 0123456789:1–15. https://doi.org/10.1007/s10340-018-1043-4
dos Santos LA, Mendes MF, Krüger AP et al (2017) Global potential distribution of Drosophila suzukii (Diptera, Drosophilidae). PLoS ONE 12(3):e0174318. https://doi.org/10.1371/journal.pone.0174318
Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130
Estoup A, Ravign V, Hufbauer R, Vitalis R, Gautier M, Facon B (2016) Is there a genetic paradox of biological invasion? Annu Rev Ecol Evol Syst 47:51–72
Farnsworth D, Hamby KA, Bolda M et al (2017) Economic analysis of revenue losses and control costs associated with the spotted wing drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Manag Sci 73(6):1083–1090. https://doi.org/10.1002/ps.4497
Ferronato P, Woch AL, Soares PL et al (2018) A phylogeographic approach to the Drosophila suzukii (Diptera: Drosophilidae) invasion in Brazil. J Econ Entomol. https://doi.org/10.1093/jee/toy321
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Fraimout A, Debat V, Fellous S, Hufbauer RA et al (2017) Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest. Mol Biol Evol 34(4):980–996. https://doi.org/10.1093/molbev/msx050
Franks SJ, Pratt PD, Tsutsui ND (2011) The genetic consequences of a demographic bottleneck in an introduced biological control insect. Conserv Genet 12(1):201–211. https://doi.org/10.1007/s10592-010-0133-5
Freda PJ, Braverman JM (2013) Drosophila suzukii, or spotted wing Drosophila, recorded in Southeastern Pennsylvania USA. Entomol News 123:71–75
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gemmell N, Akiyama S (1996) An efficient method for the extraction of DNA from vertebrate tissues. Trends Genet 12:338–339
González G, Mary AL, Goñi B (2015) Drosophila suzukii (Matsumura) found in Uruguay. Dros Inf Serv 98:103–107
Gu Z (2014) circlize implements and enhances circular visualization in R. Bioinformatics. https://doi.org/10.1093/bioinformatics/btu393
Gutierrez AP, Ponti L, Dalton DT (2016) Analysis of the invasiveness of spotted wing Drosophila (Drosophila suzukii) in North America, Europe, and the Mediterranean Basin. Biol Invasions 18:3647–3663
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67(11):1352–1357
Hopper R, Roush RT, Powell W (1993) Management of genetics of biological-control introductions. Annu Rev Entomol 38:27–51
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18. https://doi.org/10.1111/j.1365-2664.2008.01600.x
Kanzawa T (1939) Studies on Drosophila suzukii Mats: Yamanshi Prefecture Agricultural Experimental Station, Kofu, Japan. Abstr Rev Appl Entomol 29(622):49
Kirk H, Dorn S, Mazzi D (2013) Molecular genetics and genomics generate new insights into invertebrate pest invasions. Evol Appl 6(5):842–856. https://doi.org/10.1111/eva.12071
Lantschner MV, de la Vega G, Corley JC (2019) Modelling the establishment, spread and distribution shifts of pests. Int J Pest Manage 1:1. https://doi.org/10.1080/09670874.2019.1575490
Lavagnino NJ, Diaz BM, Cichón LI, de la Vega GJ et al (2018) New records of the invasive pest Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the South American continent. Rev Soc Entomol Arge 7471(1):27–31. https://doi.org/10.25085/rsea.770105
Lavrinienko A, Kesäniemi J, Watts PC et al (2017) First record of the invasive pest Drosophila suzukii in Ukraine indicates multiple sources of invasion. J Pest Sci 90(2):421–429. https://doi.org/10.1007/s10340-016-0810-3
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liebhold AM, Mccullough DG, Blackburn LM et al (2013) A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19(9):1208–1216. https://doi.org/10.1111/ddi.12112
Liebhold AM, Yamanaka T, Roques A, Augustin S (2016) Global compositional variation among native and non-native regional insect assemblages emphasizes the importance of pathways. Biol Invasions 18:893
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20(5):223–228. https://doi.org/10.1016/j.tree.2005.02.004
Mazzi D, Bravin E, Meraner M, Finger R, Kuske S (2017) Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects 8(1):18
Medina-Muñoz MC, Lucero X, Severino C et al (2015) Drosophila suzukii arrived in Chile. Dros Inf Serv 98(23):136–137
Miller MP (2005) Alleles in space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Novković B, Kimura MT (2015) Phylogeography, interaction patterns and the evolution of host choice in drosophila-parasitoid systems in Ryukyu Archipelago and Taiwan. PLoS One 10(6):e0129132
Paradis E, Jombart T, Brian K, Schliep K, Potts A (2018) Package “pegas” for R Population and Evolutionary Genetics Analysis System. Rep: CRAN. http://ape-package.ird.fr/pegas.html. V:0.11
Peakall R, Smouse P (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:855–884
Pless E, Gloria-Soria A, Evans BR et al (2017) Multiple introductions of the dengue vector, Aedes aegypti, into California. PLoS Negl Trop Dis 11(8):e0005718. https://doi.org/10.1371/journal.pntd.0005718
Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity. I. Haploid locus. Theor Appl Genet 90:462–470
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Porretta D, Canestrelli D, Bellini R, Celli G, Urbanelli S (2007) Improving insect pest management through population genetic data: a case study of the mosquito Ochlerotatus caspius (Pallas). J Appl Ecol 44(3):682–691. https://doi.org/10.1111/j.1365-2664.2007.01301.x
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramos-Onsins S, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Bio Evo 19:2092–2100
Santandino MV, Riquelme Virgala MB, Ansa MA et al (2015) Primer registro de Drosophila suzukii (Diptera: Drosophilidae) asociado al cultivo de arándanos (Vaccinium spp.) de Argentina. Rev Soc Entomol Argent 74:183–185
SENASA (2016). http://www.senasa.gob.ar/senasa-comunica/noticias/deteccion-de-drosophila-suzukii-en-la-argentina. Accessed July 2019
Soliani C, Rondan-Dueñas J, Chiappero MB et al (2010) Genetic relationships among populations of Aedes aegypti from Uruguay and northeastern Argentina inferred from ISSR-PCR data. Med Vet Entomol 24:316–323. https://doi.org/10.1111/j.1365-2915.2010.00890.x
Tait G, Grassi A, Pfab F, Crava C et al (2018) Large-scale spatial dynamics of Drosophila suzukii in Trentino, Italy. J Pest Sci 1:1–12. https://doi.org/10.1007/s10340-018-0985-x
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tuda M, Kagoshima K, Toquenaga Y, Arnqvist G (2014) Global genetic differentiation in a cosmopolitan pest of stored beans: effects of geography, host-plant usage and anthropogenic factors. PLoS One 9(9):e106268. https://doi.org/10.1371/journal.pone.0106268
Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag. 2:1–8
This work has been possible thanks to the National Service of Agri-Food Health and Quality of Argentina. We thank L. Claps for providing logistic and financial support from INTA Bariloche. A. Mattiacci and A. Falconaro helped with the figures. GJdlV is a postdoc fellow, and CS and JCC are researchers from National Scientific and Technical Research Council/Argentina (CONICET).
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Conflict of interest
All authors declare no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by A. Biondi.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
de la Vega, G.J., Corley, J.C. & Soliani, C. Genetic assessment of the invasion history of Drosophila suzukii in Argentina. J Pest Sci 93, 63–75 (2020). https://doi.org/10.1007/s10340-019-01149-x
- Spotted wing drosophila
- Invasive species
- Population genetic diversity
- Host fruit trade