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Distinct genotypes and phenotypes in European and American strains of Drosophila suzukii: implications for biology and management of an invasive organism


A clearer understanding of the structure of pest populations in newly invaded areas is a key step towards their effective management. Here, we use Drosophila suzukii as a model to highlight how populations from separate geographical regions differ in their genetic and phenotypic traits, including those associated with their invasiveness. New X-linked data indicate the presence of at most three D. suzukii genetic clusters in Europe, while North American populations are characterised by a larger genetic diversity. We found a likely new colonisation event from America to Italy and demonstrate that reference genomes from Italian and Californian populations lay in highly distant clusters. Comparative genomics indicate that these two genomes bear the traces of distinct evolutionary forces and are genetically distant, having diversified long ago in their native Asian range. Phenotypic studies further indicate that European and North American populations have differences in hatch rate, generation time, and parasitoid susceptibility. The observed genotypic and phenotypic differences likely represent a small fraction of the features unique to each of the two populations. The results provide some new insights towards both fundamental and management studies on invasive pests, particularly when findings are transferred across populations found in different geographical regions.

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  1. Adrion JR, Kousathanas A, Pascual M, Burrack HJ, Haddad NM, Bergland AO, Machado H, Sackton TB, Schlenke TA, Watada M, Wegmann D, Singh ND (2014) Drosophila suzukii: the genetic footprint of a recent, worldwide invasion. Mol Biol Evol 31:3148–3163. https://doi.org/10.1093/molbev/msu246

  2. Alexa A, Rahnenführer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600–1607. https://doi.org/10.1093/bioinformatics/btl140

  3. Asgari S, Rivers DB (2011) Venom proteins from endoparasitoid wasps and their role in host-parasite interactions. Ann Rev Entomol 56:313–335. https://doi.org/10.1146/annurev-ento-120709-144849

  4. Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang ZL, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappalá L, Desneux N (2015) Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494. https://doi.org/10.1007/s10340-015-0681-z

  5. Bastian F, Parmentier G, Roux J, Moretti S, Laudet V, Robinson-Rechavi M (2008) Bgee: integrating and comparing heterogeneous transcriptome data among species. In: Lecture notes in computer science, Springer, Berlin, pp 124–131. https://doi.org/10.1007/978-3-540-69828-9_12

  6. Birch LC (1948) The intrinsic rate of natural increase of an insect population. J Anim Ecol 17:15. https://doi.org/10.2307/1605

  7. Carton Y, Nappi AJ, Poirie M (2005) Genetics of anti-parasite resistance in invertebrates. Develop Comp Immunol 29:9–32. https://doi.org/10.1016/j.dci.2004.05.004

  8. Cattel J, Kaur R, Gibert P, Martinez J, Fraimout A, Jiggins F, Andrieux T, Siozios S, Anfora G, Miller W, Rota-Stabelli O, Mouton L (2016a) Wolbachia in European populations of the invasive pest Drosophila suzukii: regional variation in infection frequencies. PLoS ONE 11:e0147766. https://doi.org/10.1371/journal.pone.0147766

  9. Cattel J, Martinez J, Jiggins F, Mouton L, Gibert P (2016b) Wolbachia-mediated protection against viruses in the invasive pest Drosophila Suzukii. Insect Mol Biol 25:595–603. https://doi.org/10.1111/imb.12245

  10. Cattel J, Nikolouli K, Andrieux T, Martinez J, Jiggins F, Charlat S, Vavre F, Lejon D, Gibert P, Mouton L (2018) Back and forth Wolbachia transfers reveal efficient strains to control spotted wing drosophila populations. J Appl Ecol 55:2408–2418. https://doi.org/10.1111/1365-2664.13101

  11. Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L, Guidetti R (2014) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88:1–7. https://doi.org/10.1007/s10340-014-0634-y

  12. Chabert S, Allemand R, Poyet M, Eslin P, Gibert P (2012) Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol Control 63:40–47. https://doi.org/10.1016/j.biocontrol.2012.05.005

  13. Chiu JC, Jiang X, Zhao L et al (2013) Genome of Drosophila suzukii, the spotted wing drosophila. G3 Genes Genomes Genet 3:2257–2271. https://doi.org/10.1534/g3.113.008185

  14. 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. Bull Insectol 65:149–160

  15. Clemente M, Fusco G, Tonina L, Giomi F (2018) Temperature-induced phenotypic plasticity in the ovipositor of the invasive species Drosophila suzukii. J Thermal Biol 75:62–68. https://doi.org/10.1016/j.jtherbio.2018.05.001

  16. Colinet D, Deleury E, Anselme C, Cazes D, Poulain J, Azema-Dossat C, Belghazi M, Gatti JL, Poirié M (2013) Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: the case of Leptopilina parasitoids of Drosophila. Insect Biochem Mol 43:601–611. https://doi.org/10.1016/j.ibmb.2013.03.010

  17. Daane KM, Wang X, Biondi A, Miller B, Miller JC, Riedl H, Shearer PW, Guerrieri E, Giorgini M, Buffington M, van Achterberg K, Song Y, Kang T, Yi H, Jung C, Lee DW, Chung BK, Hoelmer KA, Walton VM (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835. https://doi.org/10.1007/s10340-016-0740-0

  18. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. https://doi.org/10.1111/j.1365-294x.2007.03538.x

  19. Estoup A, Ravigné V, Hufbauer R, Vitalis R, Gautier M, Facon B (2016) Is There a Genetic Paradox of Biological Invasion? Ann Rev Ecol Syst 47:51–72. https://doi.org/10.1146/annurev-ecolsys-121415-032116

  20. Fraimout A, Debat V, Fellous S et al (2017) Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest. Mol Biol Evol. https://doi.org/10.1093/molbev/msx050

  21. Fraimout A, Jacquemart P, Villarroel B, Aponte DJ, Decamps T, Herrel A, Cornette R, Debat V (2018) Phenotypic plasticity of Drosophila suzukii wing to developmental temperature: implications for flight. J Exp Biol. https://doi.org/10.1242/jeb.166868

  22. Gatti J, Schmitz A, Colinet D, Poirié M (2012) Diversity of virus-like particles in parasitoids’ venom. In: Parasitoid viruses, Elsevier, Amsterdam, pp 181–192. https://doi.org/10.1016/b978-0-12-384858-1.00015-1

  23. 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 67:1352–1357. https://doi.org/10.1002/ps.2265

  24. Haye T, Girod P, Cuthbertson AGS, Wang XG, Daane KM, Hoelmer KA, Baroffio C, Zhang JP, Desneux N (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. J Pest Science 89:643–651. https://doi.org/10.1007/s10340-016-0737-8

  25. Hickner PV, Rivaldi CL, Johnson CM, Siddappaji M, Raster GJ, Syed Z (2016) The making of a pest: insights from the evolution of chemosensory receptor families in a pestiferous and invasive fly, Drosophila suzukii. BMC Genom. https://doi.org/10.1186/s12864-016-2983-9

  26. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11):1403–1405

  27. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94

  28. Kacsoh BZ, Schlenke TA (2012) High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS ONE 7:e34721. https://doi.org/10.1371/journal.pone.0034721

  29. Kanno Y, Vokoun JC, Letcher BH (2011) Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed continuously along headwater channel networks. Mol Ecol 20:3711–3729

  30. Kaur R, Siozios S, Miller WJ, Rota-Stabelli O (2017) Insertion sequence polymorphism and genomic rearrangements uncover hidden Wolbachia diversity in Drosophila suzukii and D. subpulchrella. Sci Rep UK. https://doi.org/10.1038/s41598-017-13808-z

  31. Keightley PD, Ness RW, Halligan DL, Haddrill PR (2013) Estimation of the spontaneous mutation rate per nucleotide site in a Drosophila melanogaster full-sib family. Genetics 196:313–320. https://doi.org/10.1534/genetics.113.158758

  32. Komljenovic A, Roux J, Wollbrett J, Robinson-Rechavi M, Bastian FB (2018) BgeeDB, an R package for retrieval of curated expression datasets and for gene list expression localization enrichment tests. F1000Research 5:2748. https://doi.org/10.12688/f1000research.9973.2

  33. Kraaijeveld AR, Godfray HCJ (2003) Potential life-history costs of parasitoid avoidance in Drosophila melanogaster. Evol Ecol Res 5:1251–1261

  34. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. https://doi.org/10.1016/s0169-5347(02)02554-5

  35. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Ann Rev Entomol 52:231–253. https://doi.org/10.1146/annurev.ento.51.110104.151104

  36. Miller B, Anfora G, Buffington M, Daane KM, Dalton DT, Hoelmer KM, Rossi Stacconi MV, Grassi A, Ioriatti C, Loni A, Miller JC, Ouantar M, Wang X, Wiman NG, Walton VM (2015) Seasonal occurrence of resident parasitoids associated with Drosophila suzukii in two small fruit production regions of Italy and the USA. Bull Insectol 68(2):255–263

  37. Mitsui H, Beppu K, Kimura MT (2010) Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomol Sci 13:60–67. https://doi.org/10.1111/j.1479-8298.2010.00372.x

  38. Ometto L, Cestaro A, Ramasamy S et al (2013) Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest. Genome Biol Evol 5:745–757. https://doi.org/10.1093/gbe/evt034

  39. Pajač Živković I, Lemic D, Mešić A, Barić B, Órdenes R, Benítez HA (2018) Effect of fruit host on wing morphology in Drosophila suzukii (Diptera: Drosophilidae): A first view using geometric morphometrics. Entomol Res 48:262–268. https://doi.org/10.1111/1748-5967.12278

  40. Ramasamy S, Ometto L, Crava MC et al (2016) The evolution of olfactory gene families in Drosophila and the genomic basis of chemical-ecological adaptation in Drosophila suzukii. Genome Biol Evol 8:2297–2311. https://doi.org/10.1093/gbe/evw160

  41. Reichard M, Douda K, Przybyłski M, Popa OP, Karbanová E, Matasová K, Smith C (2015) Population-specific responses to an invasive species. P R Soc B-Biol Sci 282:1063

  42. Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242. https://doi.org/10.1016/j.tree.2014.02.003

  43. Rivero A, Vézilier J, Weill M, Read AF, Gandon S (2010) Insecticide control of vector-borne diseases: When is insecticide resistance a problem? PLoS Pathogens 6:e1001000. https://doi.org/10.1371/journal.ppat.1001000

  44. Rossi Stacconi MV, Kaur R, Mazzoni V, Ometto L, Grassi A, Gottardello A, Rota-Stabelli O, Anfora G (2016) Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues for control strategies. J Pest Sci 89:689–700. https://doi.org/10.1007/s10340-016-0753-8

  45. Rossi Stacconi MV, Panel A, Baser N, Ioriatti C, Pantezzi T, Anfora G (2017) Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biol Control 112:20–27. https://doi.org/10.1016/j.biocontrol.2017.06.003

  46. Rossi Stacconi MV, Amiresmaeili N, Biondi A et al (2018) Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing Drosophila. Biol Control 117:188–196. https://doi.org/10.1016/j.biocontrol.2017.11.013

  47. Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr Biol 23:392–398. https://doi.org/10.1016/j.cub.2013.01.026

  48. Shearer PW, West JD, Walton VM, Brown PH, Svetec N, Chiu JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecol 16(1):11

  49. Silva AX, Jander G, Samaniego H, Ramsey JS, Figueroa CC (2012) Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) I: A transcriptomic survey. PLoS ONE 7:e36366. https://doi.org/10.1371/journal.pone.0036366

  50. Strand MR (2012) Polydnavirus gene products that interact with the host immune system. In: Parasitoid viruses, Elsevier, Amsterdam, pp 149–161. https://doi.org/10.1016/b978-0-12-384858-1.00012-6

  51. Tait G, Grassi A, Pfab F et al (2018) Large-scale spatial dynamics of Drosophila suzukii in Trentino, Italy. J Pest Sci 91:1213–1224. https://doi.org/10.1007/s10340-018-0985-x

  52. Tochen S, Dalton DT, Wiman N, Hamm C, Shearer PW, Walton VM (2014) Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ Entomol 43:501–510. https://doi.org/10.1603/en13200

  53. Van Damme V, Berkvens N, Moerkens R, Berckmoes E, Wittemans L, De Vis R, Casteels H, Tirry L, De Clercq P (2014) Overwintering potential of the invasive leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) as a pest in greenhouse tomato production in Western Europe. J Pest Sci 88:533–541. https://doi.org/10.1007/s10340-014-0636-9

  54. Wiman NG, Dalton DT, Anfora G, Biondi A, Chiu JC, Daane KM, Gerdeman B, Gottardello A, Hamby KA, Isaacs R, Grassi A, Ioriatti C, Lee JC, Miller B, Rossi Stacconi MV, Shearer PW, Tanigoshi L, Wang X, Walton VM (2016) Drosophila suzukii population response to environment and management strategies. J Pest Sci 89:653–665

  55. Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15:568–573. https://doi.org/10.1093/oxfordjournals.molbev.a025957

  56. Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. https://doi.org/10.1093/molbev/msm088

  57. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43. https://doi.org/10.1093/oxfordjournals.molbev.a026236

  58. Yang Z, Nielsen R, Goldman N, Krabbe Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

  59. Zalewski A, Zalewska H, Lunneryd SG, André C, Mikusiński G (2016) Reduced genetic diversity and increased structure in American mink on the Swedish coast following invasive species control. PLoS ONE 11(6):e0157972

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Correspondence to Omar Rota-Stabelli.

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Rota-Stabelli, O., Ometto, L., Tait, G. et al. Distinct genotypes and phenotypes in European and American strains of Drosophila suzukii: implications for biology and management of an invasive organism. J Pest Sci 93, 77–89 (2020). https://doi.org/10.1007/s10340-019-01172-y

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  • Invasive insect
  • Comparative genomics
  • Population genetics
  • Parasitoid
  • Life table
  • Intraspecific variations
  • Drosophila suzukii