Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-21T20:59:09.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Old residents and new arrivals of Rhagoletis species in Europe

Published online by Cambridge University Press:  12 February 2019

A.A. Augustinos ,
C.A. Moraiti ,
E. Drosopoulou ,
I. Kounatidis ,
P. Mavragani-Tsipidou ,
K. Bourtzis  and
N.T. Papadopoulos Open the ORCID record for N.T. Papadopoulos [Opens in a new window]
A.A. Augustinos
Affiliation:
Department of Environmental and Natural Resources Management, University of Patras, Agrinio, Greece Insect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, Vienna, Austria
C.A. Moraiti
Affiliation:
Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, N. Ionia (Volos), Magnesia, Greece
E. Drosopoulou
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Faculty of Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece
I. Kounatidis
Affiliation:
Cell Biology, Development, and Genetics Laboratory, Department of Biochemistry, University of Oxford, South Park Road, Oxford OX1 3QU, UK Diamond Light Source, Harwell Science & Innovation Campus, Didcot, Oxfordshire, OX11 0DE, UK
P. Mavragani-Tsipidou
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Faculty of Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece
K. Bourtzis
Affiliation:
Insect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, Vienna, Austria
N.T. Papadopoulos*
Affiliation:
Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, N. Ionia (Volos), Magnesia, Greece
*
*Author for correspondence Phone: +302421093285 Fax: +302421093285 E-mail: nikopap@uth.gr
Get access Rights & Permissions [Opens in a new window]

Abstract

The genus Rhagoletis (Diptera: Tephritidae) comprises more than 65 species distributed throughout Europe, Asia and America, including many species of high economic importance. Currently, there are three Rhagoletis species that infest fruits and nuts in Europe. The European cherry fruit fly, Rhagoletis cerasi (may have invaded Europe a long time ago from the Caucasian area of West Asia), and two invasive species (recently introduced from North America): the eastern American cherry fruit fly, R. cingulata, and the walnut husk fly, R. completa. The presence of different Rhagoletis species may enhance population dynamics and establish an unpredictable economic risk for several fruit and nut crops in Europe. Despite their excessive economic importance, little is known on population dynamics, genetics and symbiotic associations for making sound pest control decisions in terms of species-specific, environmental friendly pest control methods. To this end, the current paper (a) summarizes recently accumulated genetic and population data for the European Rhagoletis species and their association with the endosymbiont Wolbachia pipientis, and (b) explores the possibility of using the current knowledge for implementing the innovative biological control methods of sterile insect technique and incompatible insect technique.

Keywords

Fruit fliesTephritidaemicrosatellitespolytene mapsWolbachia pipientis
Type
Review Article
Information
Bulletin of Entomological Research , Volume 109 , Issue 6 , December 2019 , pp. 701 - 712
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

First co-authors (equal contribution).

References

Aluja, M., Guillén, L., Rull, J., Höhn, H., Frey, J., Graf, B. & Samietz, J. (2011) Is the alpine divide becoming more permeable to biological invasions? – Insights on the invasion and establishment of the Walnut husk fly, Rhagoletis completa (Diptera: Tephritidae) in Switzerland. Bulletin of Entomological Research 101, 451–465.Google Scholar
Apostolaki, A., Livadaras, I., Saridaki, A., Chrysargyris, A., Savakis, C. & Bourtzis, K. (2011) Transinfection of the olive fruit fly Bactrocera oleae with Wolbachia: towards a symbiont-based population control strategy. Journal of Applied Entomology 135, 546–553.Google Scholar
Arthofer, W., Riegler, M., Schneider, D., Krammer, M., Miller, W.J. & Stauffer, C. (2009) Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 18, 3816–3830.Google Scholar
Arthofer, W., Riegler, M., Schuler, H., Schneider, D., Moder, K., Miller, W.J. & Stauffer, C. (2011) Allele intersection analysis: a novel tool for multi locus sequence assignment in multiply infected hosts. PLoS One 6, e22198.Google Scholar
Augustinos, A.A., Asimakopoulou, A.K., Papadopoulos, N.T. & Bourtzis, K. (2011) Cross-amplified microsatellites in the European cherry fly, Rhagoletis cerasi: medium polymorphic-highly informative markers. Bulletin of Entomological Research 101, 45–52.Google Scholar
Augustinos, A.A., Asimakopoulou, A.K., Moraiti, C.A., Mavragani-Tsipidou, P., Papadopoulos, N.T. & Bourtzis, K. (2014) Microsatellite and Wolbachia analysis in Rhagoletis cerasi natural populations: population structuring and multiple infections. Ecology and Evolution 4, 1943–1962.Google Scholar
Bakovic, V., Schebeck, M., Telschow, A., Stauffer, C. & Schuler, H. (2018) Spatial spread of Wolbachia in Rhagoletis cerasi populations. Biology Letters 14, 20180161.Google Scholar
Barringer, L. (2018) First record of the European cherry fruit fly, Rhagoletis cerasi (Linnaeus) (Diptera: Tephritidae), in North America. Insecta Mundi 0622, 1–14.Google Scholar
Bedo, D.G. (1986) Polytene and mitotic chromosome analysis in Ceratitis capitata (Diptera; Tephritidae). Canadian Journal of Genetics and Cytology 28, 180–188.Google Scholar
Berlocher, S.H. (1984) Genetic changes coinciding with the colonization of California by the walnut husk fly, Rhagoletis completa. Evolution 38, 906–918.Google Scholar
Berlocher, S.H. & Bush, G.L. (1982) An electrophoretic analysis of Rhagoletis (Diptera, Tephritidae) Phylogeny. Systematic Zoology 31, 136–155.Google Scholar
Boller, E. (1989) Cytoplasmatic incompatibility in Rhagoletis cerasi. pp. 69–74 in Robinson, A.S. & Hooper, G. (Eds) Fruit Flies Their Biology, Natural Enemies and Control. 3B. Amsterdam, The Netherlands, Elsevier.Google Scholar
Boller, E.F. & Bush, G.L. (1974) Evidence for genetic variation in populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae) based on physiological parameters and hybridization experiments. Entomologia Experimentalis et Applicata 17, 279–293.Google Scholar
Boller, E.F. & Prokopy, R.J. (1976) Bionomics and management of Rhagoletis. Annual Review of Entomology 21, 223–245.Google Scholar
Boller, E.F., Russ, K., Vallo, V. & Bush, G.L. (1976) Incompatible races of European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae), their origin and potential use in biological control. Entomologia Experimentalis et Applicata 20, 237–247.Google Scholar
Bourtzis, K. & Robinson, A.S. (2006) Insect pest control using Wolbachia and/or radiation. pp. 225–246, vol. 2 in Bourtzis, K. & Miller, T.A. (Eds) Insect Symbiosis. CRC Press, Boca Raton.Google Scholar
Bourtzis, K., Dobson, S.L., Xi, Z., Rasgon, J.L. & Calvitti, M. (2014) Harnessing mosquito-Wolbachia symbiosis for vector and disease control. Acta Tropica 132S, 150S–163S.Google Scholar
Bourtzis, K., Lees, R.S., Hendrichs, J. & Vreysen, M.J. (2016) More than one rabbit out of the hat: radiation, transgenic and symbiont-based approaches for sustainable management of mosquito and tsetse fly populations. Acta Tropica, 157, 115–130.Google Scholar
Brelsfoard, C.L., Clair, W.S. & Dobson, S.L. (2009) Integration of irradiation with cytoplasmic incompatibility to facilitate a lymphatic filariasis vector elimination approach. Parasites and Vectors 2, 38.Google Scholar
Bush, G.L. (1966) The taxonomy, cytology, and evolution of the genus Rhagoletis in North America (Diptera, Tephritidae). Bulletin of the Museum of Comparative Zoology 134, 431–562.Google Scholar
Bush, G.L. & Boller, E. (1977) The chromosome morphology of the Rhagoletis cerasi species complex (Diptera, Tephritidae). Annals of the Entomological Society of America 70, 316–318.Google Scholar
Bush, G.L. & Smith, J. (1998) The genetics and ecology of sympatric speciation: a case study. Researches on Population Ecology 40, 175–187.Google Scholar
Cevallos, V.E. & Nation, J.L. (2004) Chromosomes of the Caribbean fruit fly (Diptera: Tephritidae). Florida Entomologist 87, 361–364.Google Scholar
Chen, Y.H., Opp, S.B., Berlocher, S.H. & Roderick, G.K. (2006) Are bottlenecks associated with colonization? Genetic diversity and diapause variation of native and introduced Rhagoletis completa populations. Oecologia 149, 656–67.Google Scholar
Chen, Y.H., Berlocher, S.H., Opp, S.B. & Roderick, G.K. (2010) Post-colonization temporal genetic variation of an introduced fly, Rhagoletis completa. Genetica 138, 1059–1075.Google Scholar
Daniel, C. & Baker, B. (2013) Dispersal of Rhagoletis cerasi in commercial cherry orchards: efficacy of soil covering nets for cherry fruit fly control. Insects 4, 168–176.Google Scholar
Daniel, C. & Grunder, J. (2012) Integrated management of European cherry fruit fly Rhagoletis cerasi (L.): situation in Switzerland and Europe. Insects 3, 956–988.Google Scholar
Daniel, C., Mathis, S. & Feichtinger, G. (2014) A new visual trap for Rhagoletis cerasi (L.) (Diptera: Tephritidae). Insects 5, 564–576.Google Scholar
De Meyer, M., Delatte, H., Ekesi, S., Jordaens, K., Kalinova, B., Manrakhan, A., Mwatawala, M., Steck, G., Van Cann, J., Vaníčková, L., Břízová, R. & Virgilio, M. (2015) An integrative approach to unravel the Ceratitis FAR (Diptera, Tephritidae) cryptic species complex: a review. ZooKeys 540, 405–427.Google Scholar
Drew, R.A.I., Ma, J., Smith, S. & Hughes, J.M. (2011) The taxonomy and phylogenetic relationships of species in the Bactrocera musae complex of fruit flies (Diptera: Tephritidae: Dacinae) in Papua New Guinea. Raffles Bulletin of Zoology 59, 145–162.Google Scholar
Drosopoulou, E., Koeppler, K., Kounatidis, I., Nakou, I., Papadopoulos, N.T., Bourtzis, K. & Mavragani-Tsipidou, P. (2010) Genetic and cytogenetic analysis of the walnut-husk fly (Diptera: Tephritidae). Annals of the Entomological Society of America 103, 1003–1011.Google Scholar
Drosopoulou, E., Augustinos, A.A., Nakou, I., Koeppler, K., Kounatidis, I., Vogt, H., Papadopoulos, N.T., Bourtzis, K. & Mavragani-Tsipidou, P. (2011) Genetic and cytogenetic analysis of the American cherry fruit fly, Rhagoletis cingulata (Diptera: Tephritidae). Genetica 139, 1449–1464.Google Scholar
Duso, C. & Dal Lago, G. (2006) Life cycle, phenology and economic importance of the walnut husk fly Rhagoletis completa Cresson (Diptera: Tephritidae) in northern Italy. Annales de la Societe Entomologique de France 42, 245–254.Google Scholar
Dyck, V.A., Hendrichs, J. & Robinson, A.S. (2005) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.Google Scholar
Egartner, A., Zeisner, N., Hausdorf, H. & Blümel, S. (2010) First record of Rhagoletis cingulata (Loew) (Dipt., Tephritidae) in Austria. EPPO Bulletin 40, 158–162.Google Scholar
EFSA PLH Panel (EFSA Panel on Plant Health). (2014) Scientific Opinion on the pest categorisation of Rhagoletis cingulata (Loew). EFSA Journal 12(10), 3854.Google Scholar
EPPO. (2016) Rhagoletis suavis found in Berlin (DE). Reporting Service 2016/167. https://gd.eppo.int/reporting/article-5912.Google Scholar
Florian, T., Macavei, L.I., Hulujan, I.B., Vasian, I., Totos, S., Gorgan, M., Oltean, I. & Florian, V. (2018) Testing of semio-chemical products in monitoring and control of Rhagoletis cerasi L. AgroLife Scientific Journal 7, 61–68.Google Scholar
Frey, J.E., Guillén, L., Frey, B., Samietz, J., Rull, J. & Aluja, M. (2013) Developing diagnostic SNP panels for the identification of true fruit flies (Diptera: Tephritidae) within the limits of COI-based species delimitation. BMC Evolutionary Biology 13:106 https://doi.org/10.1186/1471-2148-13-106.Google Scholar
Garcia-Martinez, V., Hernandez-Ortiz, E., Zepeta-Cisneros, C.S., Robinson, A.S., Zacharopoulou, A. & Franz, G. (2009) Mitotic and polytene chromosome analysis in the Mexican fruit fly, Anastrepha ludens (Loew) (Diptera: Tephritidae). Genome 52, 20–30.Google Scholar
Glasgow, H. (1933) The host relations of our cherry fruit flies. Journal of Economic Entomology 26, 431–438.Google Scholar
Glover, M.M., Egan, S.P., Hood, G.R., Rull, J., Aluja, M. & Feder, J.L. (2018) Phylogeography of walnut-infesting Rhagoletis suavis (Diptera: Tephritidae) flies. Insect Systematics and Diversity 2, 1–9.Google Scholar
Guillén, L., Aluja, M., Rull, J., Höhn, H., Schwizer, T. & Samietz, J. (2011) Influence of walnut cultivar on infestation by Rhagoletis completa: behavioural and management implications. Entomologia Experimentalis et Applicata 140, 207–217.Google Scholar
Johannesen, J., Keyghobadi, N., Schuler, H., Stauffer, C. & Vogt, H. (2013) Invasion genetics of American cherry fruit fly in Europe and signals of hybridization with the European cherry fruit fly. Entomologia Experimentalis et Applicata, 147, 61–72.Google Scholar
Karimi, J. & Darsouei, R. (2014) Presence of the endosymbiont Wolbachia among some fruit flies (Diptera: Tephritidae) from Iran: a multilocus sequence typing approach. Journal of Asia-Pacific Entomology 17, 105–112.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.Google Scholar
Kovanci, O.B. & Kovanci, B. (2006) Effect of altitude on seasonal flight activity of Rhagoletis cerasi flies (Diptera: Tephritidae). Bulletin of Entomological Research 96, 345–351.Google Scholar
Kozánek, M., Semelbauer, M. & Bartoš, R. (2018) The first finding of walnut husk fly Rhagoletis completa (Diptera, Tephritidae) in Slovakia. Folia Faunistica Slovaca 22, 29–31.Google Scholar
Krosch, M.N., Schutze, M.K., Armstrong, K.F., Boontop, Y., Bonkin, L.M., Chapman, T.A., Englezou, A., Cameron, S.L. & Clarke, A.R. (2013) Piecing together an integrative taxonomic puzzle: microsatellite, wing shape and aedeagus length analyses of Bactrocera dorsalis s.l. (Diptera: Tephritidae) find no evidence of multiple lineages in a proposed contact zone along the Thai/Malay Peninsula. Systematic Entomology 38, 2–13.Google Scholar
Lanzavecchia, S.B., Juri, M., Bonomi, A., Gomulski, L., Scannapieco, A.C., Segura, D.F., Malacrida, A., Cladera, J.L. & Gasperi, G. (2014) Microsatellite markers from the ‘South American fruit fly’ Anastrepha fraterculus: a valuable tool for population genetic analysis and SIT applications. BMC Genetic, 15 (Suppl 2), S13.Google Scholar
Mateos, M., Martinez, H., Lanzavecchia, S.B., Conte, C., Guillén, K., Morán-Aceves, B., Toledo, J., Liedo, P., Asimakis, E.D., Doudoumis, V., Kyritsis, G.A., Papadopoulos, N.T., Avgoustinos, A.A., Segura, D.E., Tsiamis, G. & Bourtzis, K. (2019) Wolbachia pipientis associated to tephritid fruit fly pests: from basic research to applications. BioRxiv, https://doi.org/10.1101/358333 (in press).Google Scholar
Matolin, S. (1976) Mechanism causing incompatibility between different strains of Rhagoletis cerasi (Diptera, Tephritidae). Acta Entomologica Bohemoslovaca 73, 289–292.Google Scholar
Mavragani-Tsipidou, P., Karamanlidou, G., Zacharopoulou, A., Koliais, S. & Kastritsis, C. (1992) Mitotic and polytene chromosome analysis in Dacus oleae (Diptera: Tephritidae). Genome 35, 373–378.Google Scholar
Maxwell, S.A., Rasic, G. & Keyghobadi, N. (2009) Characterization of microsatellite loci for the western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae). Molecular Ecology Resources 9, 1025–1028.Google Scholar
Moraiti, C.A. & Papadopoulos, N.T. (2017) Obligate annual and successive facultative diapause establish a bet-hedging strategy of Rhagoletis cerasi (Diptera: Tephritidae) in seasonally unpredictable environments. Physiological Entomology 42, 225–231.Google Scholar
Moraiti, C.A., Nakas, C.T., Köppler, K. & Papadopoulos, N.T. (2012 a) Geographical variation in adult life-history traits of the European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae). Biological Journal of the Linnean Society 107, 137–152.Google Scholar
Moraiti, C.A., Nakas, C.T. & Papadopoulos, N.T. (2012 b) Prolonged pupal dormancy is associated with significant fitness cost for adults of Rhagoletis cerasi (Diptera: Tephritidae). Journal of Insect Physiology 58, 1128–1135.Google Scholar
Moraiti, C.A., Nakas, C.T. & Papadopoulos, N.T. (2014) Diapause termination of Rhagoletis cerasi pupae is regulated by local adaptation and phenotypic plasticity: escape in time through bet-hedging strategies. Journal of Evolutionary Biology 27, 43–54.Google Scholar
Moraiti, C.A., Nakas, C.T. & Papadopoulos, N.T. (2017) Local adaptation, intrapopulation adult emergence patterns, sex and prolonged diapause regulate the rate of postwinter development in pupae of the European cherry fruit fly. Biological Journal of the Linnean Society 121, 282–293.Google Scholar
Nikolouli, K., Colinet, H., Renault, D., Enriquez, T., Mouton, L., Gibert, P., Sassu, F., Cáceres, P., Stauffer, C., Pereira, R. & Bourtzis, K. (2018) Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii. Journal of Pest Science 91, 489–503.Google Scholar
Nježić, B., Pećanin, D. & Đurić, G. (2017) Improvement of management of Rhagoletis cerasi in Bosnia and Herzegovina based on a phenological model. Proceedings of the Latvian Academy of sciences. Section B 71, 229–232.Google Scholar
O'Neill, S.L., Giordano, R., Colbert, A.M.E., Karr, T.L. & Robertson, H.M. (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proceedings of the National Academy of Sciences of the USA 89, 2699–2702.Google Scholar
Ostojic, I., Zovko, M. & Petrovic, D. (2014) First record of walnut husk fly Rhagoletis completa (Cresson, 1929) in Bosnia and Herzegovina. Works of the Faculty of Agriculture University of Sarajevo 59, 121–126.Google Scholar
Papanastasiou, S.A., Nestel, D., Diamantidis, A.D., Nakas, C.T. & Papadopoulos, N.T. (2011) Physiological and biological patterns of a highland and a coastal population of the European cherry fruit fly during diapause. Journal of Insect Physiology 57, 83–93.Google Scholar
Procunier, W.S. & Smith, J.J. (1993) Localization of ribosomal DNA in Rhagoletis pomonella (Diptera: Tephritidae) by in situ hybridization. Insect Molecular Biology 2, 163–174.Google Scholar
Qin, Y.-J., Buahom, N., Krosch, M.N., Du, Y., Wu, Y., Malacrida, A.R., Deng, Y.-L., Liu, J.-Q., Jiang, X.-L. & Li, Z.-H. (2016) Genetic diversity and population structure in Bactrocera correcta (Diptera: Tephritidae) inferred from mtDNA cox1 and microsatellite markers. Scientific Reports 6, 38476.Google Scholar
Ramírez, C.C., Salazar, M., Palma, R.E., Cordero, C. & Meza-Basso, L. (2008) Phylogeographical analysis of Neotropical Rhagoletis (Diptera: Tephritidae): did the Andes uplift contribute to current morphological differences? Neotropical Entomology 37, 651–661.Google Scholar
Riegler, M. & Stauffer, C. (2002) Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 11, 2425–2434.Google Scholar
Robinson, A.S., Franz, G. & Fisher, K. (1999) Genetic sexing strains in the medfly, Ceratitis capitata: Development, mass rearing and field application. Trends in Entomology 2, 81–104.Google Scholar
Rull, J., Aluja, M. & Feder, J.L. (2011) Distribution and Basic Biology of Black cherry-infesting Rhagoletis (Diptera: Tephritidae) in México. Annals of the Entomological Society of America 104, 202–211.Google Scholar
Rull, J., Tadeo, E., Aluja, M., Guillén, L., Egan, S.P. & Feder, L.J. (2012) Hybridization and sequential components of reproductive isolation between parapatric walnut-infesting sister species Rhagoletis completa and Rhagoletis zoqui. Biological Journal of the Linnean Society 107, 886–898.Google Scholar
Saridaki, A. & Bourtzis, K. (2010) Wolbachia: more than just a bug in insects genitals. Current Opinion in Microbiology 13, 67–72.Google Scholar
Schneider, D.I., Riegler, M., Arthofer, W., Merçot, H., Egan, S.P. & Feder, L.J. (2013) Uncovering Wolbachia diversity upon artificial host transfer. PloS One 8, e82402.Google Scholar
Schuler, H., Arthofer, W., Krumböck, S., Köppler, K., Vogt, H., Teixeira, L.A.F., Riegler, M. & Stauffer, C. (2009) The bacterial endosymbiont Wolbachia in the invasive cherry fruit fly Rhagoletis cingulata (Diptera, Tephritidae). Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 17, 99–101.Google Scholar
Schuler, H., Arthofer, W., Riegler, M., Bertheau, C., Krumböck, S., Köppler, K., Vogt, H., Teixeira, L.A.F. & Stauffer, C. (2011) Multiple Wolbachia infections in Rhagoletis pomonella. Entomologia Experimentalis et Applicata 139, 138–144.Google Scholar
Schuler, H., Arthofer, W., Krumbock, S., Bertheau, C. & Stauffer, C. (2012) Wolbachia infection in the Walnut-Husk fly Rhagoletis completa Cresson 1929 (Diptera: Tephritidae). Mitteilungen der Deutschen Gesellschaft fur Allgemeine und Angewandte Entomologie 18, 243–245.Google Scholar
Schuler, H., Bertheau, C., Egan, S.P., Feder, J.L., Riegler, M., Schlick-Steiner, B.C., Steiner, F.M., Johannesen, J., Kern, P., Tuba, K., Lakatos, F., Köppler, K., Arthofer, W. & Stauffer, C. (2013) Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Molecular Ecology 22, 4101–4111.Google Scholar
Schwarz, D., McPheron, B.A., Hartl, G.B., Boller, E.F. & Hoffmeister, T.S. (2003) A second case of genetic host races in Rhagoletis? A population genetic comparison of sympatric host populations in the European cherry fruit fly, Rhagoletis cerasi. Entomologia Experimentalis et Applicata 108, 11–17.Google Scholar
Smith, J.J. & Bush, G.L. (1997) Phylogeny of the genus Rhagoletis (Diptera: Tephritidae) inferred from DNA sequences of mitochondrial cytochrome oxidase II. Molecular Phylogenetics and Evolution 7, 33–43.Google Scholar
Smith, J.J. & Bush, G.L. (2000) Phylogeny of the subtribe Carpomyina (Trypetinae), emphasizing relationships of the genus Rhagoletis. pp. 187–217 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL. CRC Press.Google Scholar
Smith, J.J., Jaycox, M., Smith-Caldas, M.R.B. & Bush, G.L. (2005) Analysis of mitochondrial DNA and morphological characters in the subtribe Carpomyina (Diptera: Tephritidae). Israel Journal of Entomology 35-36, 317–340.Google Scholar
Smith, J.J., Powell, T.H.Q., Teixeira, L., Armstrong, W.O., McClowry, R.J., Isaacs, R., Hood, G.R., Feder, L.J. & Gut, L. (2014) Genetic structure of cherry fruit fly (Rhagoletis cingulata) populations across managed, unmanaged, and natural habitats. Entomologia Experimentalis et Applicata 150, 157–165.Google Scholar
Vallo, V., Remund, U. & Boller, E.F. (1976) Storage conditions of stockpiled diapausing pupae of Rhagoletis cerasi for obtaining high emergence rates. Entomophaga 21, 251–256.Google Scholar
Velez, S., Taylor, M.S., Noor, M.A.F., Lobo, N.F. & Feder, J.L. (2006) Isolation and characterization of microsatellite loci from the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae). Molecular Ecology Notes 6, 90–92.Google Scholar
Verheggen, F., Verhaeghe, A., Giordanengo, P., Tassus, X. & Escobar-Gutiérrez, A. (2017) Walnut husk fly, Rhagoletis completa (Diptera: Tephritidae), invades Europe: invasion potential and control strategies. Applied Entomology and Zoology 52, 1–7.Google Scholar
Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews. Microbiology 6, 741–51.Google Scholar
White, I.M. & Elson-Harris, M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Wallingford, Oxfordshire, CABI.Google Scholar
Yee, W.L., Hernández-Ortiz, V., Rull, J., Sinclair, B.J. & Neven, L.G. (2014) Status of Rhagoletis (Diptera: Tephritidae) pests in the NAPPO countries. Journal of Economic Entomology 107, 11–28.Google Scholar
Zabalou, S., Riegler, M., Theodorakopoulou, M., Stauffer, C., Savakis, C. & Bourtzis, K. (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proceedings of the National Academy of Sciences of the United States of America 101, 15042–15045.Google Scholar
Zabalou, S., Apostolaki, A., Livadaras, I., Franz, G., Robinson, A.S., Savakis, C. & Bourtzis, K. (2009) Incompatible insect technique: incompatible males from a Ceratitis capitata genetic sexing strain. Entomologia Experimentalis et Applicata 132, 232–240.Google Scholar
Zacharopoulou, A. (1987) Cytogenetic analysis of mitotic and salivary gland chromosomes in the medfly Ceratitis capitata. Genome 29, 67–71.Google Scholar
Zacharopoulou, A., Augustinos, A.A., Sayed, W.A.A., Robinson, A.S. & Franz, G. (2011 a) Mitotic and polytene chromosomes analysis of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Genetica 139, 79–90.Google Scholar
Zacharopoulou, A., Sayed, W.A.A., Augustinos, A.A., Yesmin, F., Robinson, A.S. & Franz, G. (2011 b) Analysis of mitotic and polytene chromosomes and photographic polytene chromosome maps in Bactrocera cucurbitae (Diptera: Tephritidae). Annals of the Entomological Society of America 104, 306–318.Google Scholar
Zacharopoulou, A., Augustinos, A.A., Drosopoulou, E., Tsoumani, K.T., Gariou-Papalexiou, A., Franz, G., Mathiopoulos, K.D., 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. Entomologia Experimentalis et Applicata 164, 204–225.Google Scholar
Zhang, D., Lees, R.S., Xi, Z., Gilles, J.R. & Bourtzis, K. (2015 a) Combining the sterile insect technique with Wolbachia-based approaches: II – A safer approach to Aedes albopictus population suppression programmes, designed to minimize the consequences of inadvertent female release. PLoS One 10, e0135194.Google Scholar
Zhang, D., Zheng, X., Xi, Z., Bourtzis, K. & Gilles, J.R. (2015 b) Combining the sterile insect technique with the incompatible insect technique: I – Impact of Wolbachia infection on the fitness of triple and double-infected strains of Aedes albopictus. PLoS One 10, e0121126.Google Scholar
Zhang, D., Lees, R.S., Xi, Z., Bourtzis, K. & Gilles, J.R. (2016) Combining the sterile insect technique with the incompatible insect technique: III – Robust mating competitiveness of irradiated triple Wolbachia-infected Aedes albopictus males under semi-field conditions. PLoS One 11, e0151864.Google Scholar
Zug, R. & Hammerstein, P. (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PloS One 7, e38544.Google Scholar