Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-28T20:53:22.815Z Has data issue: false hasContentIssue false

Mosquitoes of the Anopheles maculipennis group (Diptera: Culicidae) in Romania, with the discovery and formal recognition of a new species based on molecular and morphological evidence

Published online by Cambridge University Press:  09 March 2007

G. Nicolescu
Affiliation:
Department of Medical Entomology, Cantacuzino Institute, Bucharest, Romania
Y.-M. Linton
Affiliation:
Mosquitoes Programme and Biomedical Sciences Theme, Department of Entomology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
A. Vladimirescu
Affiliation:
Department of Medical Entomology, Cantacuzino Institute, Bucharest, Romania
T.M. Howard
Affiliation:
Mosquitoes Programme and Biomedical Sciences Theme, Department of Entomology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
R.E. Harbach*
Affiliation:
Mosquitoes Programme and Biomedical Sciences Theme, Department of Entomology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
*
*Fax: 00442079425229 E-mail: [email protected]

Abstract

Mosquitoes of the Anopheles maculipennis group were collected in five districts of Romania (Constanta, Giurgiu, Ilfov, Mehedinti and Suceava) between March 2000 and June 2003. Two hundred and ninety-seven specimens were identified by molecular methods. Nuclear rDNA ITS2 sequences of 178 specimens were compared with GenBank sequences for nine known Palaearctic species of the group, and 119 specimens were identified using an ITS2 PCR–RFLP assay developed during the study. Five genetically distinct species of the group were identified: A. atroparvus van Thiel, A. maculipennis Meigen, A. melanoon Hackett and A. messeae Falleroni and a previously unrecognized species. The new species, herein formally described and named A. daciaesp. n., was collected in the Black Sea coastal region and plains adjacent to the Danube River in southern Romania. Anopheles daciae is most similar to and sympatric with A. messeae. It is contrasted with A. messeae and characterized on the basis of unique nuclear ITS2 and mitochondrial COI DNA sequences and morphological characters of the eggs. The larval, pupal and adults stages of the two species were also compared, but no reliable characters were found to distinguish them. It seems likely that A. daciae is more widespread in eastern Europe and the Balkan States, and could be responsible for malaria transmission in these regions that is currently attributed to A. messeae. Anopheles melanoon is reported from Romania for the first time.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2004

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.)

References

Alten, B., Caglar, S.S., Özel, O. (2000) Malaria and its vectors in Turkey. European Mosquito Bulletin 7, 2733.Google Scholar
Boccolini, D., Di Luca, M., Marinucci, .M, Romi, R. (2003) Further molecular and morphological support for the formal synonymy of Anopheles subalpinus Hackett & Lewis with A. melanoon Hackett. European Mosquito Bulletin 16, 15.Google Scholar
Bruce-Chwatt, L.J., de Zulueta, J. (1980) The rise and fall of malaria in Europe. London: Butler and Tanner.Google Scholar
Cianchi, R., Sabatini, A., Boccolini, D., Bullini, L., Coluzzi, M. (1987) Electrophoretic evidence of reproductive isolation between sympatric populations of Anopheles melanoon and A. subalpinus. p. 1560 in Third International Congress on Malaria and Babesiosis International Laveran Foundation, Annecy France.Google Scholar
Clary, D.O. & Wolstenholme, D.R. (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organisation and genetic code. Journal of Molecular Evolution 22, 252271.CrossRefGoogle ScholarPubMed
Collins, F.H. & Paskewitz, S.M. (1996) A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Molecular Biology 5, 19.CrossRefGoogle ScholarPubMed
Di Luca, M., Boccolini, D., Marinucci, M., Romi, R. (2004) Intrapopulation polymorpism in Anophyelas messeae (An. masulipennis complex) inferred by molecular analysis. Journal of Medical Entomology 41, 582586.CrossRefGoogle Scholar
Falleroni, D. (1926) Fauna anofelica italiana e suo “habitat” (paludi, risaie, canali). Metodi di lotta contro la malaria. Rivista di Malariologia 5, 553593.Google Scholar
Frizzi, G. (1953) Etude cytogenetique d' Anopheles maculipennis en Italie. Bulletin of the World Health Organization 9, 335344.Google Scholar
Gordeev, M., Goriacheva, I., Shaikevitch, E., Ejov, M. (2004) Intraspecific variability of the second internal transcribed spacer of the ribosomal DNA among five Palaearctic species of anopheline mosquitoes. European Mosquito Bulletin 17, 1419.Google Scholar
Hackett, L.W. (1934) The present status of our knowledge of the sub-species of Anopheles maculipennis. Transactions of the Royal Society of Tropical Medicine and Hygiene 28, 109128.CrossRefGoogle Scholar
Hackett, L.W. & Lewis, D.J. (1935) A new variety of Anopheles maculipennis in southern Europe. Rivista di Malariologia 14, 377383.Google Scholar
Harbach, R.E. & Knight, K.L. (1980) Taxonomists' glossary of mosquito anatomy Plexus Publishing Inc., Marlton New Jersey.Google Scholar
International Commission on Zoological Nomenclature. (1999) International code of zoological nomenclature 4th edn. The International Trust for Zoological Nomenclature London.Google Scholar
Jetten, T.H., Takken, W. (1994) Anophelism without malaria in Europe. A review of the ecology and distribution of the genus Anopheles in Europe. Wageningen Agricultural University Papers, 94–5. Agricultural University Wageningen, The Netherlands.Google Scholar
Kitzmiller, J.B., Frizzi, G., Baker, R. (1967) Evolution and speciation within the maculipennis complex of the genus Anopheles. Genetics of insect vectors of disease. pp. 151210 in Wright, J.W., Pal, R. (Eds) LondonElsevier Publishing.Google Scholar
Kumar, S., Tamura, K., Jakobsen, I.B., Nei, M. (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 12441245.Google Scholar
Linton, Y.-M., Samanidou-Voyadjoglou, A., Smith, L. & Harbach, R.E. (2001a) New occurrence records for Anopheles maculipennis and An. messeae in northern Greece based on DNA sequence data. European Mosquito Bulletin 11, 3136.Google Scholar
Linton, Y.-M., Harbach, R.E., Chang, M.S., Anthony, T.G., Matusop, A. (2001b) Morphological and molecular identity of Anopheles (Cellia) sundaicus (Diptera: Culicidae), the nominotypical member of a malaria vector species complex in Southeast Asia. Systematic Entomology 26, 357366.Google Scholar
Linton, Y.-M., Samanidou-Voyadjoglou, A. & Harbach, R.E. (2002a) Ribosomal ITS2 sequence data for Anopheles maculipennis and An. messeae in northern Greece, with a critical assessment of previously published sequences. Insect Molecular Biology 11, 379383.CrossRefGoogle Scholar
Linton, Y.-M., Smith, L. & Harbach, R.E. (2002b) Molecular confirmation of sympatric populations of Anopheles messeae and Anopheles atroparvus overwintering in Kent, southeast England. European Mosquito Bulletin 13, 816.Google Scholar
Linton, Y.-M., Smith, L. & Harbach, R.E. (2002c) Observations on the taxonomic status of Anopheles subalpinus Hackett & Lewis and An. melanoon Hackett. European Mosquito Bulletin 13, 17.Google Scholar
Linton, Y.-M., Smith, L., Koliopoulos, G., Samanidou-Voyadjoglou, A., Zounos, A.K. & Harbach, R.E. (2003) Morphological and molecular characterization of Anopheles (Anopheles) maculipennis Meigen, type species of the genus and nominotypical member of the Maculipennis Complex. Systematic Entomology 28, 3656.Google Scholar
Linton, Y.-M., Smith, L., Koliopoulos, G., Zounos, A.K., Samanidou-Voyadjoglou, A., Patsoula, E. & Harbach, R.E. (2004) The Anopheles maculipennis complex (Diptera: Culicidae) in Greece. Medical and Veterinary Entomology 18 (in press).Google Scholar
Marinucci, M., Romi, R., Mancini, P., Di Luca, M., Severini, C. (1999) Phylogenetic relationships of seven Palaearctic members of the maculipennis complex inferred from ITS2 sequence data. Insect Molecular Biology 8, 469480.CrossRefGoogle Scholar
Martini, E., Zotta, G. (1934) Rapport sur un voyage d'études effectué à travers la Roumanie pendant les mois d'Août et de Septembre 1933. Races d' A. maculipennis en Roumanie. Societé des Nations, C.H. (Malaria) 218, 384.Google Scholar
Missiroli, A. (1939) The varieties of Anopheles maculipennis and the malaria problem in Italy. Proceedings of the 7th International Congress of Entomology 3, 16191640.Google Scholar
Nicolescu, G. (1995) The mosquitoes of Romania: an annotated checklist and bibliography. Romanian Archives of Microbiology and Immunology 54, 75109.Google Scholar
Nicolescu, G. (1996) George Zotta (1886–1942): an early concept of malaria stratification. Romanian Archives of Microbiology and Immunology 2, 173179.Google Scholar
Nikolaeva, N. (1996) Resurgence of malaria in the former Soviet Union (FSU). Society of Vector Ecology Newsletter 27, 1011.Google Scholar
Proft, J., Maier, W.A., Kampen, H. (1999) Identification of six sibling species of the Anopheles maculipennis complex (Diptera: Culicidae) by a polymerase chain reaction assay. Parasitology Research 85, 837843.Google Scholar
Romi, R., Boccolini, D., Hovanesyan, I., Grigoryan, G., Di Luca, M., Sabatinelli, G. (2002) Anopheles sacharovi (Diptera: Culicidae): a re-emerging malaria vector in the Ararat Valley of Armenia. Journal of Medical Entomology 39, 446450.Google Scholar
Sedaghat, M.M., Linton, Y.-M., Nicolescu, G., Smith, L., Koliopoulos, G., Zounos, A.K., Oshaghi, M.A., Vatandoost, H. & Harbach, R.E. (2003a) Morphological and molecular characterization of Anopheles (Anopheles) sacharovi Favre, a primary vector of malaria in the Middle East. Systematic Entomology 28, 241256.CrossRefGoogle Scholar
Sedaghat, M.M., Linton, Y.-M., Oshaghi, M.A., Vatandoost, H. & Harbach, R.E. (2003b) The Anopheles maculipennis complex (Diptera: Culicidae) in Iran: molecular characterization and recognition of a new species. Bulletin of Entomological Research 93, 527535.Google Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Lui, H., Flook, P. (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651701.CrossRefGoogle Scholar
Stegnii, V.N. (1982) Genetic adaptation and speciation in sibling species of the Eurasian Maculipennis Complex. pp. 454465 in Steiner, W.M., Tabachnick, W.J., Rai, K.S., Narang, S. (Eds) Recent developments in the genetics of insect vectors, Champaign: Illinois Stipes Publishing.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.CrossRefGoogle Scholar
White, G.B. (1978) Systematic reappraisal of the Anopheles maculipennis complex. Mosquito Systematics 10, 1344.Google Scholar
Zotta, G. (1938) Contribution à l'étude de la distribution des races d' A. maculipennis en rapport avec les grandes lignes de repartition du paludisme en Roumanie. Archives Roumaines de Pathologie Expérimentale et de Microbiologie 2, 209246.Google Scholar
Zotta, G., Georgescu, M., Ionescu, V., Lupascu, G., Mardare, I. & Teodorescu, A.M. (1940) Nouvelle carte de la disribution des races d' Anopheles en Roumanie. Bulletin de la Section Scientifique de l'Académie Roumaine 2, 7387.Google Scholar