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The chromosomes of Drosophila suzukii (Diptera: Drosophilidae): detailed photographic polytene chromosomal maps and in situ hybridization data

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Abstract

The spotted wing drosophila, D. suzukii, is a serious agricultural pest attacking a variety of soft fruits and vegetables. Although originating from East Asia it has recently invaded America and Europe raising major concern about its expansion potential and the consequent economic losses. Since cytogenetic information on the species is scarce, we report here the mitotic karyotype and detailed photographic maps of the salivary gland polytene chromosomes of D. suzukii. The mitotic metaphase complement contains three pairs of autosomes, one of which is dot-like, and one pair of heteromorphic (XX/XY) sex chromosomes. The salivary gland polytene complement consists of five long polytene arms, representing the two metacentric autosomes and the acrocentric X chromosome, and one very short polytene element, which corresponds to the dot-like autosome. Banding pattern as well as the most characteristic features and prominent landmarks of each polytene chromosome arm are presented and discussed. Furthermore, twelve gene markers have been mapped on the polytene chromosomes of D. suzukii by in situ hybridization. Their distribution pattern was found quite similar to that of D. melanogaster revealing conservation of synteny although the relative position within each chromosome arm for most of the genes differed significantly between D. suzukii and D. melanogaster. The chromosome information presented here is suitable for comparative cytogenetic studies and phylogenetic exploration, while it could also facilitate the assembly of the genome sequence and support the development of genetic tools for species-specific and environment-friendly biological control applications such as the sterile insect technique.

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References

  • Ashburner M (1989) Inversions. In: Ashburner M (ed) Drosophila: a laboratory handbook. Cold Spring Harbor Laboratory Press, New York, pp 509–528

    Google Scholar 

  • Ashburner M, Carson HL, Thompson J (1982) The genetics and biology of Drosophila. Academic Press, London

    Google Scholar 

  • 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 88:469–494. https://doi.org/10.1007/s10340-015-0681-z

    Article  Google Scholar 

  • Atallah J, Teixeira L, Salazar R, Zaragoza G, Kopp A (2014) The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proc Biol Sci 281:20132840. https://doi.org/10.1098/rspb.2013.2840

    Article  PubMed  PubMed Central  Google Scholar 

  • Augustinos AA, Drosopoulou E, Gariou-Papalexiou A, Bourtzis K, Mavragani-Tsipidou P, Zacharopoulou A (2014) The Bactrocera dorsalis species complex: comparative cytogenetic analysis in support of Sterile Insect Technique applications. BMC Genet 15(Suppl 2):S16

    PubMed  PubMed Central  Google Scholar 

  • Augustinos AA, Drosopoulou E, Gariou-Papalexiou A, Asimakis ED, Cáceres C, Tsiamis G, Bourtzis K, Mavragani-Tsipidou P, Zacharopoulou A (2015) Cytogenetic and symbiont analysis of five members of the B. dorsalis complex (Diptera, Tephritidae): no evidence of chromosomal or symbiont-based speciation events. ZooKeys 540:273–298

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhutkar A, Schaeffer SW, Russo SM et al (2008) Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes. Genetics 179:1657–1680

    PubMed  PubMed Central  Google Scholar 

  • Bolda M, Goodhue R, Zalom FG (2010) Spotted wing Drosophila: potential economic impact of a newly established pest. Agric Resour Econ Update 13:5–8

    Google Scholar 

  • Burrack HJ, Smith JP, Pfeiffer DG, Koehler G, La Forest J (2012) Using volunteer-based networks to track Drosophila suzukii (Diptera: Drosophilidae) an invasive pest of fruit crops. J Integr Pest Manag 4:B1–B5

    Google Scholar 

  • Caceres C, Segura DF, Vera MT, Wornoayporn V, Cladera JL, Teal P, Sapountzis P, Bourtzis K, Zacharopoulou A, Robinson AS (2009) Incipient speciation revealed in Anastrepha fraterculus (Diptera; Tephritidae) by studies on mating compatibility, sex pheromones, hybridization, and cytology. Biol J Linnean Soc 97:152–165. https://doi.org/10.1111/j.1095-8312.2008.01193.x

    Article  Google Scholar 

  • Calabria G, Maca J, Bachli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147

    Google Scholar 

  • Campos SRC, Rieger TT, Santos JF (2007) Homology of polytene elements between Drosophila and Zaprionus determined by in situ hybridization in Zaprionus indianus. Genet Mol Res 6:262–276

    CAS  PubMed  Google Scholar 

  • Chiu JC, Jiang X, Zhao L, Hamm CA, Cridland JM et al (2013) Genome of Drosophila suzukii, the spotted wing Drosophila. G3: Genes Genom Genet 3:2257–2271. https://doi.org/10.1534/g3.113.008185

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Clark AG, Eisen MB, Smith DR et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    PubMed  Google Scholar 

  • Coluzzi M, Sabatini A, della Torre A, Di Deco MA, Petrarca V (2002) A polytene chromosome analysis of the Anopheles gambiae species complex. Science 298:1415–1418

    CAS  PubMed  Google Scholar 

  • Deng Q, Zeng Q, Qian Y, Li C, Yang Y (2007) Research on the karyotype and evolution of Drosophila melanogaster species group. J Genet Genomics 34:196–213. https://doi.org/10.1016/S1673-8527(07)60021-6

    Article  PubMed  Google Scholar 

  • 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 87:379–383. https://doi.org/10.1007/s10340-014-0591-5

    Article  Google Scholar 

  • Drosopoulou E, Scouras ZG (1995) The β-tubulin gene family evolution in the Drosophila montium subgroup of the melanogaster species group. J Mol Evol 41:293–298

    CAS  PubMed  Google Scholar 

  • Drosopoulou E, Scouras ZG (1998) The organization of the α-tubulin gene family in the Drosophila montium subgroup of the melanogaster species group. Genome 41:504–509

    CAS  PubMed  Google Scholar 

  • Drosopoulou E, Konstantopoulou I, Scouras ZG (1996) The heat shock genes in the Drosophila montium subgroup. Chromosomal localization and evolutionary implications. Chromosoma 105:104–110

    CAS  PubMed  Google Scholar 

  • Drosopoulou E, Tsiafouli M, Mavragani-Tsipidou P, Scouras ZG (1997) The glutamate dehydrogenase, E74 and putative actin gene loci in the Drosophila montium subgroup. Chromosoma 106:20–28

    CAS  PubMed  Google Scholar 

  • Drosopoulou E, Wiebauer K, Yiangou M, Mavragani-Tsipidou P, Domdey H, Scouras ZG (2002) Isolation, characterization, and localization of beta tubulin genomic clones of three Drosophila montium subgroup species. Genome 45:604–607

    CAS  PubMed  Google Scholar 

  • Drosopoulou E, Augustinos AA, Nakou I, Koeppler K, Kounatidis I, Vogt H, Papadopoulos NT, Bourtzis K, Mavragani-Tsipidou P (2011a) Genetic and cytogenetic analysis of the American cherry fruit fly, Rhagoletis cingulata (Diptera: Tephritidae). Genetica 139:1449–1464. https://doi.org/10.1007/s10709-012-9644-y

    Article  PubMed  Google Scholar 

  • Drosopoulou E, Nestel D, Nakou I, Kounatidis I, Papadopoulos NT, Bourtzis K, Mavragani-Tsipidou P (2011b) Cytogenetic analysis of the Ethiopian fruit fly Dacus ciliatus (Diptera: Tephritidae). Genetica 139:723–732

    CAS  PubMed  Google Scholar 

  • Drosopoulou E, Nakou I, Mavragani-Tsipidou P (2015) The Bactrocera oleae genome: localization of nine genes on the polytene chromosomes of the olive fruit fly (Diptera: Tephritidae). Genome 57:573–576

    Google Scholar 

  • Drosopoulou E, Pantelidou C, Gariou-Papalexiou A, Augustinos AA, Chartomatsidou T, Kyritsis GA, Bourtzis K, Mavragani-Tsipidou P, Zacharopoulou A (2017) The chromosomes and the mitogenome of Ceratitis fasciventris (Diptera: Tephritidae): two genetic approaches towards the Ceratitis FAR species complex resolution. Sci Rep 7:4877. https://doi.org/10.1038/s41598-017-05132-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyck VA, Hendrichs J, Robinson AS (2005) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, The Netherlands

    Google Scholar 

  • Foster G, Whitten M, Konovalov C, Arnold J, Maffi G (1981) Autosomal genetic maps of the Australian sheep blowfly, Lucilia cuprina dorsalis R.-D. (Diptera: Calliphoridae), and possible correlations with the linkage maps of Musca domestica L. and Drosophila melanogaster (Mg.). Genet Res 37:55–69

    Google Scholar 

  • Garcia C, Delprat A, Ruiz A, Valente VLS (2015) Reassignment of Drosophila willistoni genome scaffolds to chromosome II arms. G3: Genes Genom Genet 5:2559–2566

    CAS  Google Scholar 

  • Gariou-Papalexiou A, Gourzi P, Delprat A, Kritikou D, Rapti K, Chrysanthakopoulou B, Mintzas A, Zacharopoulou A (2002) Polytene chromosomes as tools in the genetic analysis of the Mediterranean fruit fly, Ceratitis capitata. Genetica 116:59–71

    CAS  PubMed  Google Scholar 

  • Gariou-Papalexiou A, Yannopoulos G, Robinson AS, Zacharopoulou A (2007) Polytene chromosome maps in four species of tsetse flies Glossina austeni, G. pallidipes, G. morsitans morsitans and G. m. submorsitans (Diptera: Glossinidae): a comparative analysis. Genetica 129:243–251

    CAS  PubMed  Google Scholar 

  • Gariou-Papalexiou A, Giardini MC, Augustinos AA, Drosopoulou E, Lanzavecchia SB, Cladera JL, Caceres C, Bourtzis K, Mavragani-Tsipidou P, Zacharopoulou A (2016) Cytogenetic analysis of the south American fruit fly Anastrepha fraterculus (Diptera: Tephritidae) species complex: construction of detailed photographic polytene chromosome maps of the Argentinian Af. sp.1 member. PLOS One 11(6):7192. https://doi.org/10.1371/journal.pone.0157192

    Article  CAS  Google Scholar 

  • Goldberg DA (1980) Isolation and partial characterization of the Drosophila alcohol dehydrogenase gene. Proc Natl Acad Sci USA 77:5794–5798. https://doi.org/10.1073/pnas.77.10.5794

    Article  CAS  PubMed  Google Scholar 

  • Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG (2011) Spotted wing Drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Manag Sci 67:1396–1402. https://doi.org/10.1002/ps.2259

    Article  CAS  PubMed  Google Scholar 

  • Grassi A, Giongo L, Palmieri L (2011) Drosophila (Sophophora) suzukii (Matsumura), new pest of soft fruits in Trentino (North-Italy) and in Europe. IOBC/WPRS Bull 70:121–128

    Google Scholar 

  • Hamby KA, Hernandez A, Boundy-Mills K, Zalom FG (2012) Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Appl Environ Microbiol 78:4869–4873

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 Sci 89:643–651. https://doi.org/10.1007/s10340-016-0737-8

    Article  Google Scholar 

  • Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149

    CAS  PubMed  Google Scholar 

  • Ioriatti C, Walton V, Dalton D, Anfora G, Grassi A, Maistri S, Mazzoni V (2015) Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions. J Econ Entomol 108:1148–1155. https://doi.org/10.1093/jee/tov042

    Article  CAS  PubMed  Google Scholar 

  • Kalfayan L, Wensink PC (1981) α-tubulin genes of Drosophila. Cell 24:97–106

    CAS  PubMed  Google Scholar 

  • Konstantopoulou I, Scouras ZG (1998) The heat-shock gene hsp83 of Drosophila auraria: genomic organization, nucleotide sequence, and long antiparallel coupled ORFs (LAC ORFs). J Mol Evol 46:334–343

    CAS  PubMed  Google Scholar 

  • Konstantopoulou I, Ouzounis C, Drosopoulou E, Yiangou M, Sideras P, Sander C, Scouras ZG (1995) A Drosophila hsp70 gene contains long antiparallel coupled open reading frames (LAC ORFs) conserved in homologous loci. J Mol Evol 41:414–420

    CAS  PubMed  Google Scholar 

  • Krimbas CB, Powell JR (1992) Drosophila inversion polymorphism. CRC Press, Florida

    Google Scholar 

  • Lee JC, Bruck DJ, Dreves AJ, Ioriatti C, Vogt H, Baueld P (2011) In focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Manag Sci 67:1349–1351

    CAS  PubMed  Google Scholar 

  • Lee Y, Collier TC, Sanford MR, Marsden CD, Fofana A, Cornel AJ, Lanzaro GC (2013) Chromosome inversions, genomic differentiation and speciation in the African Malaria Mosquito Anopheles gambiae. PLOS One. https://doi.org/10.1371/journal.pone.0057887

    Article  PubMed  PubMed Central  Google Scholar 

  • Lemeunier F, Ashburner M (1984) Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). IV. The chromosomes of two new species. Chromosoma 89(343):351

    Google Scholar 

  • Lemeunier F, David JR, Tsacas L, Ashburner M (1986) The melanogaster species group. In: Ashburner M, Carson HL, Thompson J (eds) The genetics and biology of Drosophila, vol 3. Academic Press, London, pp 147–256

    Google Scholar 

  • Matsumura S (1931) 6000 illustrated insects of Japan-empire (in Japanese). Tokohshoin, Tokyo

    Google Scholar 

  • Mavragani-Tsipidou P (2002) Genetic and cytogenetic analysis of the olive fruit fly Bactrocera oleae (Diptera: Tephritidae). Genetica 116:45–57

    CAS  PubMed  Google Scholar 

  • Mavragani-Tsipidou P, Scouras ZG, Charalampidis K, Lavrentiadou S, Kastritsis CD (1992) The polytene chromosomes of Drosophila triauraria and D. quadraria, sibling species of D. auraria. Genome 35:318–326

    CAS  PubMed  Google Scholar 

  • Mavragani-Tsipidou P, Zacharopoulou A, Drosopoulou E, Augustinos AA, Bourtzis K, Marec F (2014) Tephritid Fruit Flies (Diptera). In: Sharakhov I (ed) Protocols for cytogenetic mapping of Arthropod genomes. CRC Press, Taylor and Francis Group, pp 1–62

    Google Scholar 

  • Pardali E, Feggou E, Drosopoulou E, Konstantopoulou I, Scouras ZG, Mavragani-Tsipidou P (1996) The Afrotropical Drosophila montium subgroup: Balbiani ring 1, polytene chromosomes, and heat shock response of Drosophila vulcana. Genome 39:588–597

    CAS  PubMed  Google Scholar 

  • Pardue ML (1986) Drosophila a practical approach. In: Roberts DB (ed) In situ hybridization to DNA of chromosomes and nuclei. IRL Press, Oxford, pp 111–137

    Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358

    PubMed  Google Scholar 

  • Schaeffer SW, Bhutkar AU, McAllister BF et al (2008) Polytene chromosomal maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps. Genetics 179:1601–1655

    PubMed  PubMed Central  Google Scholar 

  • Sharakhov IV, Artemov GN, Sharakhova MV (2016) Chromosome evolution in malaria mosquitoes inferred from physically mapped genome assemblies. J Bioinform Comput Biol 14:1630003. https://doi.org/10.1142/S0219720016300033

    Article  CAS  PubMed  Google Scholar 

  • Sharakhova M, Hammond MP, Lobo NF, Krzywinski J, Unger MF, Hillenmeyer ME et al (2007) Update of the Anopheles gambiae PEST genome assembly. Genome Biol 8:R5

    PubMed  PubMed Central  Google Scholar 

  • Stocker AJ, Rusuwa BB, Blacket MJ, Frentiu FD, Sullivan M et al (2012) Physical and linkage maps for Drosophila serrata, a model species for studies of clinal adaptation and sexual selection. G3-Genes Genom Genet 2:287–297. https://doi.org/10.1534/g3.111.001354

    Article  Google Scholar 

  • Sturtevant AH, Novitski E (1941) The homologies of the chromosome elements in the genus Drosophila. Genetics 24:517–541

    Google Scholar 

  • Sved JA, Chen Y, Shearman D, Frommer M, Gilchrist AS, Sherwin WB (2016) Extraordinary conservation of entire chromosomes in insects over long evolutionary periods. Evolution 70:229–234

    PubMed  Google Scholar 

  • Thurmond J, Goodman JL, Strelets VB, Attrill H, Gramates LS, Marygold SJ, Matthews BB, Millburn M, Antonazzo G, Trovisco V, Kaufman TC, Calvi BR, FlyBase Consortium (2019) FlyBase 2.0: the next generation. Nucleic Acids Res 47(D1):D759–D765

    CAS  PubMed  Google Scholar 

  • Tsoumani KT, Augustinos AA, Kakani EG, Drosopoulou E, Mavragani-Tsipidou P, Mathiopoulos KD (2011) Isolation, annotation and applications of expressed sequence tags from the olive fly, Bactrocera oleae. Mol Genet Genomics 285:33–45

    CAS  PubMed  Google Scholar 

  • Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O’Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:1–7

    Google Scholar 

  • Yang Y, Zhang YP, Qian YH, Zeng QT (2004) Phylogenetic relationships of the Drosophila melanogaster species group deduced from spacer regions of histone gene H2A. Mol Phylogenet Evol 30:336–343

    CAS  PubMed  Google Scholar 

  • Yang Y, Hou ZH, Qian YH, Kang H, Zeng Q-T (2012) Increasing the data size to accurately reconstruct the phylogenetic relationships between nine subgroups of the Drosophila melanogaster species group (Drosophilidae, Diptera). Mol Phylogenet Evol 62:214–223

    PubMed  Google Scholar 

  • Zacharopoulou A, Franz G (2013) Genetic and Cytogenetic Characterization of Genetic Sexing Strains of Bactrocera dorsalis and Bactrocera cucurbitae (Diptera: Tephritidae). J Econ Entomol 106:995–1003

    CAS  PubMed  Google Scholar 

  • Zacharopoulou A, Frisardi M, Savakis C, Robinson AS, Tolias P, Konsolaki M, Komitopoulou K, Kafatos FC (1992) The genome of the Mediterranean fruit fly Ceratitis capitata: localization of molecular markers by in situ hybridization to salivary gland polytene chromosomes. Chromosoma 101:448–455

    CAS  PubMed  Google Scholar 

  • Zacharopoulou A, Augustinos AA, Sayed WAA, Robinson AS, Franz G (2011a) Mitotic and polytene chromosomes analysis of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Genetica 139:79–90

    PubMed  Google Scholar 

  • Zacharopoulou A, Sayed WAA, Augustinos AA, Yesmin F, Robinson AS, Franz G (2011b) Analysis of mitotic and polytene chromosomes and photographic polytene chromosome maps in Bactrocera cucurbitae (Diptera: Tephritidae). Ann Entomol Soc Am 104:306–318

    Google Scholar 

  • Zacharopoulou A, Augustinos AA, Drosopoulou E, Tsoumani K, Gariou-Papalexiou A, Franz G, Mathiopoulos KD, Bourtzis K, Mavragani-Tsipidou P (2017) A review of more than 30 years of cytogenetic studies of Tephritidae in support of Sterile Insect Technique and global trade. Entomol Exp Appl 164:204–225. https://doi.org/10.1111/eea.12616

    Article  Google Scholar 

  • Zambetaki A, Zacharopoulou A, Scouras ZG, Mavragani-Tsipidou P (1999) The genome of the olive fruit fly Bactrocera oleae: localization of molecular markers by in situ hybridization to the salivary gland polytene chromosomes. Genome 42:744–751. https://doi.org/10.1139/g99-017

    Article  CAS  Google Scholar 

  • Zhao JT, Frommer M, Sved JA, Zacharopoulou A (1998) Mitotic and polytene chromosome analyses in the Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae). Genome 41:510–526

    CAS  PubMed  Google Scholar 

  • Zhimulev IF, Belayaeva ES, Semeshin VF et al (2004) Polytene chromosomes: 70 years of genetic research. Internat Rev Cytol 241:203–275

    CAS  Google Scholar 

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Acknowledgements

We would like to thank Katerina Nikolouli for providing the biological material used in the present study and Prof. Penelope Mavragani-Tsipidou for fruitful discussions on the results of the present work. The present study has been funded by the Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture through CRP and SSA projects.

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Correspondence to Elena Drosopoulou.

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Drosopoulou, E., Gariou-Papalexiou, A., Karamoustou, E. et al. The chromosomes of Drosophila suzukii (Diptera: Drosophilidae): detailed photographic polytene chromosomal maps and in situ hybridization data. Mol Genet Genomics 294, 1535–1546 (2019). https://doi.org/10.1007/s00438-019-01595-3

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