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Cytogenetic analysis of the Ethiopian fruit fly Dacus ciliatus (Diptera: Tephritidae)

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Abstract

The Ethiopian fruit fly, Dacus ciliatus, is an important pest of cucurbits, which recently invaded the Middle East. The genetics and cytogenetics of D. ciliatus have been scarcely studied. Such information is, however, an essential basis for understanding the biology of insect pests, as well as for the design of modern control strategies. We report here the mitotic karyotype and detailed photographic maps of the salivary gland polytene chromosomes of this species. The mitotic metaphase complement consists of six pairs of chromosomes, including one pair of heteromorphic sex (XX/XY) chromosomes. The heterogametic sex is ascribed to the male. The analysis of the salivary gland polytene complement shows a total number of five long chromosomes (10 polytene arms), which correspond to the five autosomes of the mitotic nuclei, and a heterochromatic mass corresponding to the sex chromosomes. Banding patterns, as well as the most characteristic features and prominent landmarks of each polytene chromosome are presented and discussed. Chromosomal homologies between D. ciliatus and Bactrocera oleae are proposed by comparing chromosome banding patterns and by in situ hybridization of the hsp70 gene.

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References

  • Akhtaruzzaman M, Alam MZ, Sardar MA (1999) Identification and distribution of fruit flies infesting cucurbits in Bangladesh. Bangladesh J Entomol 9:93–101

    Google Scholar 

  • Baimai V, Trinachartvanit W, Tigvattananont S, Grote PJ, Poramarcom R, Kijchalao U (1995) Metaphase karyotypes of fruit flies of Thailand. I. Five sibling species of the Bactrocera dorsalis complex (Diptera: Tephritidae). Genome 38:1015–1022

    Article  PubMed  CAS  Google Scholar 

  • Baimai V, Phinchongsakuldit J, Trinachartvanit W (1999) Metaphase karyotypes of fruit flies of Thailand (III). Six members of the Bactrocera dorsalis complex. Zool Stud 38:110–118

    Google Scholar 

  • Baimai V, Phinchongsakuldit J, Sumrandee C (2000) Cytological evidence for a complex of species within the taxon Bactrocera tau (Diptera: Tephritidae) in Thailand. Biol J Linn Soc 69:399–409

    Article  Google Scholar 

  • Bedo DG (1982) Differential sex chromosome replication and dosage compensation in polytene trichogen cells of Lucilia cuprina (Diptera: Calliphoridae). Chromosoma 87:21–32

    Article  PubMed  CAS  Google Scholar 

  • Bedo DG (1986) Polytene and mitotic chromosome analysis in Ceratitis capitata (Diptera; Tephritidae). Can J Genet Cytol 28:180–188

    Google Scholar 

  • Bedo DG (1987) Polytene chromosome mapping in Ceratitis capitata (Diptera: Tephritidae). Genome 29:598–611

    Article  Google Scholar 

  • Bedo DG (1992) Polytene chromosomes of the Old World screwworm fly (Chrysomya bezziana) and its evolutionary relationships with Lucilia cuprina and Cochiliomyia hominivorax (Diptera: Calliphoridae). Genome 35:294–303

    Article  PubMed  CAS  Google Scholar 

  • Bedo DG, Zacharopoulou A (1988) Intertissue variability of polytene chromosome banding patterns. Trends Genet 4:90–91

    Article  PubMed  CAS  Google Scholar 

  • Belyaeva ES, Demakov SA, Pokholkova GV, Alekseyenko AA, Kolesnikova TD, Zhimulev IF (2006) DNA underreplication in intercalary heterochromatin regions in polytene chromosomes of Drosophila melanogaster correlates with the formation of partial chromosomal aberrations and ectopic pairing. Chromosoma 115:355–366

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar S, Kaul D, Chaturvedi R (1980) Chromosomal studies in three species of the genus Dacus (Trypetidae: Diptera). Genetica 54:11–15

    Article  Google Scholar 

  • Braig HR, Zhou W, Dobson SL, O’Neill SL (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol 180:2373–2378

    PubMed  CAS  Google Scholar 

  • Bush GL (1962) The cytotaxonomy of the larvae of some Mexican fruit flies in the genus Anastrepha (Tephritidae, Diptera). Psyche Stuttg 69:87–101

    Article  Google Scholar 

  • Bush GL, Boller F (1977) Chromosome morphology of Rhagoletis cerasi species complex (Diptera, Tephritidae). Ann Entomol Soc Am 70:316–318

    Google Scholar 

  • Cáceres C, Segura DF, Vera MT, Wornoayporn W, Cladera JL, Teal P, Sapountzis P, Bourtzis K, Zacharopoulou A, Robinson AS (2009) Incipient speciation revealed in Anastrepha fraterculus by studies on mating compatibility, sex pheromones, hybridization and cytology. Biol J Linn Soc 97:152–165

    Article  Google Scholar 

  • Cevallos VE, Nation JL (2004) Chromosomes of the Caribbean fruit fly (Diptera: Tephritidae). Fla Entomol 87:361–364

    Article  Google Scholar 

  • Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033

    Article  PubMed  CAS  Google Scholar 

  • Childress D (1969) Polytene chromosomes and linkage group-chromosome correlations in the Australian sheep blowfly Lucilia cuprina (Diptera: Calliphoridae). Chromosoma 26:208–214

    Article  PubMed  CAS  Google Scholar 

  • Davies N, Roderick GK (2005) Dipteran sex chromosomes in evolutionary developmental biology. In: Wiegmann BM, Yeates DK (eds) The evolutionary biology of flies. Johns Hopkins University Press, Baltimore, pp 196–216

    Google Scholar 

  • Drew RAI (1989) The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Mem Qld Mus 26:521

    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

    Article  PubMed  CAS  Google Scholar 

  • Drosopoulou E, Chrysopoulou A, Nikita V, Mavragani-Tsipidou P (2009) The heat shock 70 genes of the olive pest Bactrocera oleae: genomic organization and molecular characterization of a transcription unit and its proximal promoter region. Genome 52:210–214

    Article  PubMed  CAS  Google Scholar 

  • Drosopoulou E, Koeppler K, Kounatidis I, Nakou I, Papadopoulos NT, Bourtzis K, Mavragani-Tsipidou P (2010) Genetic and cytogenetic analysis of the Walnut-Husk fly (Diptera: Tephritidae). Ann Entomol Soc Am 103:1003–1011

    Article  Google Scholar 

  • Eichler EE, Sankoff D (2003) Structural dynamics of Eukaryotic chromosome evolution. Science 301:793–797

    Article  PubMed  CAS  Google Scholar 

  • Engels WR, Preston CR (1981) Identifying P factors in Drosophila by means of chromosome breakage hotspots. Cell 26:421–428

    Article  PubMed  CAS  Google Scholar 

  • Engels WR, Preston CR (1984) Formation of chromosome rearrangements by P factors in Drosophila. Genetics 107:657–678

    PubMed  CAS  Google Scholar 

  • European and Mediterranean Plant Protection Organization [EPPO] (2006) Distribution maps of quarantine pests for Europe, Dacus ciliatus. http://www.eppo.org/QUARANTINE/insects/Dacus_ciliatus/DACUCI_map.htm

  • Foster GG, Whitten MJ, Konovalov C, Bedo DG, Maddern RH, Boon DT (1980) Cytogenetic studies of Lucilia cuprina dorsalis R.-D. (Diptera: Calliphoridae). Polytene chromosome maps of the autosomes and cytogenetic localization of visible genetic markers. Chromosoma 81:151–168

    Article  Google Scholar 

  • Foster GG, Whitten MJ, Konovalov C, Arnold JTA, Maffi G (1981) Autosomal genetics maps of the Australian sheep blow fly Lucilia cuprina dorsalis (Diptera: Calliphoridae) and possible correlations with linkage maps of Musca domestica and Drosophila melanogaster. Genet Res 37:55–70

    Article  Google Scholar 

  • Frias D (2002) Importance of larval morphology and heterochromatic variation in the identification and evolution of sibling species in the genus Rhagoletis (Diptera: Tephritidae) in Chile. In: Barnes BN (ed) Proceedings, 6th international symposium on fruit flies of economic importance, 6–10, Stellenbosch. Isteg Scientific Publications, Irene, pp 267–276

  • Frias L (1992) Aspetos de la biologia evolutiva de especies de Tephritidae (Diptera) de distribucion chilena Acta Ent. Chilena 17:67–79

    Google Scholar 

  • Frydrychova R, Marec F (2002) Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115:179–187

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Martinez V, Hernandez-Ortiz E, Zepeta-Cisneros CS, Robinson AS, Zacharopoulou A, Franz G (2009) Mitotic and polytene chromosome analysis in the Mexican fruit fly, Anastrepha ludens (Loew) (Diptera: Tephritidae). Genome 52:20–30

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Gopalan HB (1972) The study of somatic, meiotic and salivary gland chromosomes of melon fly, Dacus cucurbitae. Caryologia 25:163–172

    Google Scholar 

  • Han HY, McPheron BA (1997) Molecular phylogenetic study of Tephritidae (Insecta: Diptera) using partial sequences of the mitochondrial 16S ribosomal DNA. Mol Phylogenet Evol 7:17–32

    Article  PubMed  CAS  Google Scholar 

  • Han HY, Ro KE (2009) Molecular phylogeny of the family Tephritidae (Insecta: Diptera): new insight from combined analysis of the mitochondrial 12S, 16S, and COII genes. Mol Cells 27:55–66

    Article  PubMed  CAS  Google Scholar 

  • Hancock DL (1989) Southern Africa. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control, World crop pests, vol 3A. Elsevier Science Publishers B.V., Amsterdam, pp 51–58

  • Hunwattanakul N, Baimai V (1994) Mitotic karyotype of four species of fruit flies (Bactrocera) in Thailand. Kasetsart J Nat Sci 28:142–148

    Google Scholar 

  • Kaiser VB, Bachtrog D (2010) Evolution of sex chromosomes in insects. Annu Rev Genet 44:91–112

    Article  PubMed  CAS  Google Scholar 

  • Kapoor VC (1993) Indian fruit flies. Oxford & IBH Publishing Co. PVT LTD, New Delhi

    Google Scholar 

  • Kastritsis CD, Scouras ZG, Ashburner M (1986) Duplications in the polytene chromosomes of Drosophila auraria. Chromosoma 93:381–385

    Article  Google Scholar 

  • Kounatidis I, Papadopoulos N, Bourtzis K, Mavragani-Tsipidou P (2008) Genetic and cytogenetic analysis of the fruit fly Rhagoletis cerasi (Diptera: Tephritidae). Genome 51:479–491

    Article  PubMed  Google Scholar 

  • Krimbas CB (1963) A contribution to the cytogenetics of Dacus oleae (Gmel) (Diptera: Trypetidae): the salivary gland and the mitotic chromosomes. Caryologia 16:371–376

    Google Scholar 

  • Krimbas CB, Powell JR (1992) Drosophila inversion polymorphisms. CRC Press, Boca Raton

    Google Scholar 

  • Lehman N, Pfrender ME, Morin PA, Crease TJ, Lynch M (1995) A hierarchical molecular phylogeny within the genus Daphnia. Mol Phylogenet Evol 4:395–407

    Article  PubMed  CAS  Google Scholar 

  • Mahmood R, Murtaza M, Kazimi SK (1996) Notes on the biology of fruit flies of economic importance in Pakistan. In: 2nd international congress of entomological sciences (Abstracts). Islamabad, pp 10–11

  • Maklakov A, Ishaaya I, Freidberg A, Yawetz A, Horowitz AR, Yaron I (2001) Toxicological studies of organophosphate and pyrethroid insecticides for controlling the fruit fly Dacus ciliatus (Diptera: Tephritidae). J Econ Entomol 94:1059–1066

    Article  PubMed  CAS  Google Scholar 

  • Malacrida A, Gasperi G, Biscaldi GF, Milani R (1986) Persistence of linkage relationships among enzyme loci in some Dipteran species. Atti Assoc Genet Ital 31:121–122

    Google Scholar 

  • Mavragani-Tsipidou P (2002) Genetic and Cytogenetic Analysis of Bactrocera oleae (Dacus oleae) (Diptera: Tephritidae). Genetica 116:45–57

    Article  PubMed  CAS  Google Scholar 

  • Mavragani-Tsipidou P, Karamanlidou G, Zacharopoulou A, Koliais S, Kastritsis CD (1992) Mitotic and polytene chromosome analysis in Dacus oleae (Diptera: Tephritidae). Genome 35:373–378

    Article  PubMed  CAS  Google Scholar 

  • Michailova P, Ilkova J, Petrova N, White K (2001) Rearrangements in the salivary gland chromosomes of Chironomus riparius Mg. (Diptera, Chironomidae) following exposure to lead. Caryologia 54:349–363

    Google Scholar 

  • Michailova P, Ilkova J, Hankeln T, Schmidt ER, Selvaggi A, Zampicinini G, Sella G (2009) Somatic breakpoints, distribution of repetitive DNA and non-LTR retrotransposon insertion sites in the chromosomes of Chironomus piger Strenzke (Diptera, Chironomidae). Genetica 135:137–148

    Article  PubMed  CAS  Google Scholar 

  • O’Neill SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699–2702

    Article  PubMed  Google Scholar 

  • Pardue ML, Gall JG (1975) Nucleic acid hybridization to the DNA of cytological preparations. Methods Cell Biol 10:1–16

    Article  PubMed  CAS  Google Scholar 

  • Radu M, Rössler Y, Koltin Y (1975) The chromosomes of the Mediterranean fruit fly Ceratitis capitata (Wied): karyotype and chromosomal organization. Cytologia (Tokyo) 40:823–828

    Google Scholar 

  • Segura MD, Callejas C, Fernandez MP, Ochando MD (2006) New contributions towards the understanding of the phylogenetic relationships among economically important fruit flies (Diptera: Tephritidae). Bull Entomol Res 96:279–288

    Article  PubMed  CAS  Google Scholar 

  • Selivon D, Perondini ALP (1997) Evaluation of techniques for C and ASG banding of the mitotic chromosomes of Anastrepha species (Diptera, Tephritidae). Braz J Genet 20:651–653

    Google Scholar 

  • Selivon D, Perondini ALP, Rocha LS (2005) Systematics, morphology and physiology—Karyotype characterization of Anastrepha fruit flies (Diptera: Tephritidae). Neotrop Entomol 34:273–279

    Article  Google Scholar 

  • Shahjahan RM, Yesmin F (2002) Polytene chromosome maps of the melon fly Bactrocera curcubitae (Diptera, Tephritidae). Genome 45:1167–1174

    Article  PubMed  CAS  Google Scholar 

  • Singh OP, Gupta JP (1984) Studies on mitotic and salivary chromosomes of Dacus curcubitae Coquilett (Diptera, Tephritidae). Genetica 62:217–221

    Article  Google Scholar 

  • Smith PT, Kambhampati S, Armstrong KA (2003) Phylogenetic relationships among Bactrocera species (Diptera: Tephritidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 26:8–17

    Article  PubMed  CAS  Google Scholar 

  • Solferini VN, Morgante JS (1987) Karyotype study of eight species of Anastrepha (Diptera; Tephritidae). Caryology 40:229–241

    Google Scholar 

  • Solferini VN, Morgante JS (1990) X1X1X2X2:X1X2Y mechanism of sex determination in Anastrepha bistrigata A. serpentine (Diptera; Tephritidae). Rev Bras Genet 13:201–208

    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 Xy, Bactrocera oleae. Mol Genet Genomics 285:33–45

    Article  PubMed  CAS  Google Scholar 

  • Vaissiere BE, Froissart R (1996) Pest management and pollination of cantaloupes grown under spunbounded row cover in West Africa. J Hort Sci 71:755–766

    Google Scholar 

  • White IM (2000) Morphological features of the Dacini (Dacinae): their significance to behavior and classification. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, pp 505–533

    Google Scholar 

  • White IM, Elson-Harris MM (eds) (1992) Dacus (Didacus) ciliatus Loew. In: Fruit flies of economic significance: their identification and bionomics. CAB International, Wallingford, pp 329–331

  • Zacharopoulou A (1987) Cytogenetic analysis of mitotic and salivary gland chromosomes in the medfly Ceratitis capitata. Genome 29:67–71

    Article  Google Scholar 

  • Zacharopoulou A (1990) Polytene chromosome maps in the medfly Ceratitis capitata. Genome 33:184–197

    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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zambetaki A, Kleanthous K, Mavragani-Tsipidou P (1995) Cytogenetic analysis of Malpighian tubule and salivary gland polytene chromosomes of Bactrocera oleae (Dacus oleae) (Diptera: Tephritidae). Genome 38:1070–1081

    Article  PubMed  CAS  Google Scholar 

  • Zambetaki A, Pasteur N, Mavragani-Tsipidou P (1998) Cytogenetic analysis of Malpighian tubule polytene chromosomes of Culex pipiens (Diptera: Culicidae). Genome 41:751–755

    Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Zhimulev IF, Belayaeva ES, Semeshin VF, Koryakov DE, Demakov SA, Demakova OV, Pokholkova GV, Andreyeva EN (2004) Polytene chromosomes: 70 years of genetic research. Int Rev Cytol 241:203–275

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, Rousset F, O’Neill S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond B Biol Sci 265:509–515

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Ian White (Natural History Museum, UK) and Marc De Meyer (Royal Museum for Central Africa, Belgium) for discussing the phylogenetic relationships of Dacinae.

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Drosopoulou, E., Nestel, D., Nakou, I. et al. Cytogenetic analysis of the Ethiopian fruit fly Dacus ciliatus (Diptera: Tephritidae). Genetica 139, 723–732 (2011). https://doi.org/10.1007/s10709-011-9575-z

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