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Multi-character approach reveals a discordant pattern of phenotypic variation during ontogeny in Culex pipiens biotypes (Diptera: Culicidae)

Published online by Cambridge University Press:  26 November 2014

B. Krtinić ,
J. Ludoški  and
V. Milankov
B. Krtinić
Affiliation:
Ciklonizacija, Primorska 76, 21000 Novi Sad, Serbia
J. Ludoški
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000 Novi Sad, Serbia
V. Milankov*
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000 Novi Sad, Serbia
*
*Author for correspondence Phone: +381 21 485 2671 Fax: +381 21 450 620 E-mail: vesna.milankov@dbe.uns.ac.rs
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Abstract

Culex (Culex) pipiens s.l. (Diptera: Culicidae) comprises two distinct biotypes, pipiens (‘rural’) and molestus (‘urban’), both of which are thought to have differing capacities due to different host preferences. To better understand West Nile encephalitis epidemiology and improve risk assessment, local distinction between these forms is essential. This study assesses phenotypic variation at larval and adult stages of ‘urban’ and ‘rural’ biotypes of the species by complementary use of meristic, univariate and multivariate traits analyzed by traditional and geometric morphometrics. Third- and fourth-instar larvae from a broad area of the city of Novi Sad (Serbia) were collected and reared in the laboratory. After adult eclosion, the sex of each larva was recorded based on the sex of the corresponding adult. Examination of the association between variations of larval traits revealed contrasting variations regarding pecten spines vs. siphonal size and siphonal shape in the ‘rural’ biotype. Siphons of larvae collected in marshes and forest ecosystems outside urban areas were found to be the largest, but possessed the smallest number of pecten spines. In addition, statistically significant female-biased sexual dimorphism was observed in siphonal size, wing size and wing shape. Finally, we propose that an integrative approach is essential in delimitation of Cx. pipiens s.l. biotypes, since their differentiation was not possible based solely on larval and adult traits. Our findings shed light on the phenotypic plasticity important for population persistence in the changing environment of these medically important taxa.

Keywords

diagnostic traitslarval traitssexual dimorphismwing trait variation
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 1 , February 2015 , pp. 129 - 138
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Copyright
Copyright © Cambridge University Press 2014 

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References

Adams, D.C., Rohlf, F.J. & Slice, D.E. (2004) Geometric morphometrics: ten years of progress following the “revolution”. Italian Journal of Zoology 71, 5–16.Google Scholar
Atkinson, C.T., Woods, K.L., Dusek, R.J., Sileo, L.S. & Iko, W.M. (1995) Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimently infected iiwi (Vestaria coccinea). Parasitology 111, 59–69.Google Scholar
Ayala, D., Fontaine, M.C., Cohuet, A., Fontenille, D., Vitalis, R. & Simard, F. (2011) Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus . Molecular Biology and Evolution 28, 745–758.Google Scholar
Aytekin, S., Aytekin, A.M. & Alten, B. (2009) Effect of different larval rearing temperatures on the productivity (Ro) and morphology of the malaria vector Anopheles superpictus Grassi (Diptera: Culicidae) using geometric morphometrics. Journal of Vector Ecology 43(1), 32–42.CrossRefGoogle Scholar
Bahnck, C.M. & Fonseca, D.M. (2006) Rapid assay to identify the two genetic forms of Culex (Culex) pipiens L. (Diptera: Culicidae) and hybrid populations. American Journal of Tropical Medicine and Hygiene 75, 251–255.Google Scholar
Becker, N., Petrić, D., Zgomba, M., Boase, C., Dahl, C., Lane, J. & Kaiser, A. (2010) Mosquitoes and their Control. 2nd edn. Berlin, Heidelberg, Springer Verlag.Google Scholar
Bookstein, F.L. (1991) Morphometric Tools for Landmark Data. New York, Cambridge University Press.Google Scholar
Byrne, K. & Nichols, R.A. (1999) Culex pipiens in London underground tunnels: differentiation between surface and subterranean population. Heredity 82, 7–15.CrossRefGoogle Scholar
Chevillon, C., Eritja, R., Pasteur, N. & Raymond, M. (1995) Commensalism adaption and gene flow: mosquitoes from the Culex pipiens complex in different habitats. Genetics Research 66, 147–157.CrossRefGoogle ScholarPubMed
Chevillon, C., Rivet, Y., Raymond, M., Rousset, F., Smouse, P.E. & Pasteur, N. (1998) Migration/selection balance and ecotypic differentiation in the mosquito Culex pipiens . Molecular Ecology 7, 197–208.CrossRefGoogle Scholar
Clements, A.N. (1992) The Biology of Mosquitoes. I. Development, Nutrition and Reproduction. London, Chapman & Hall, p. 509.Google Scholar
Demirci, B., Lee, Y., Lanzaro, C.G. & Alten, B. (2012) Altitudinal genetic and morphometric variation of Culex theileri Theobald (Diptera: Culicidae) from northeastern Turkey. Journal of Vector Ecology 37(1), 197–209.Google Scholar
Dhivya, R. & Manimegalai, K. (2013) Wing Shape Analysis of the Japanese encephalitis vector Culex gelidus (Diptera: Culicidae) at the Foot Hill of Southern Western Ghats, India. World Journal of Zoology 8(1), 119–125.Google Scholar
Dujardin, J.P. (2011) Modern morphometrics of medically important insects, chapter 16. pp. 474–501 in Tibayrenc, M. (Ed.) Genetics and Evolution of Infectious Diseases. Elsevier Insights, London, UK.Google Scholar
Eritja, R. & Aranda, K. (1995) Preliminary observations on sex-related variation in morphological character of Culex pipiens (Diptera: Culicidae) larvae in northeastern Spain. Mosquito Systematics 27(2), 73–77.Google Scholar
Farajollahi, A., Fonseca, D.M., Kramer, L.D. & Kilpatrick, A.M. (2011) ‘‘Bird biting’’ mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infection, Genetics and Evolution 11, 1577–1585.CrossRefGoogle ScholarPubMed
Farid, H.A., Hammad, R.E., Hassan, M.M., Morsy, Z.S., Kamal, I.H., Weil, G.J. & Ramzy, R.M.R. (2001) Detection of Wuchereria bancrofti in mosquitoes by the polymerase chain reaction: a potentially useful tool for large-scale control programmes. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 29–32.Google Scholar
Fonseca, D.M., Keyghobadi, N., Malcolm, C.A., Mehmet, C., Schaffner, F., Mogi, M., Fleischer, R.C. & Wilkerson, R.C. (2004) Emerging vectors in the Culex pipiens complex. Science 303, 1535–1538.Google Scholar
Fonseca, D.M., LaPointe, D. & Fleischer, R.C. (2000) Bottlenecks and multiple introductions: population genetics of Culex quinquefasciatus, the vector of avian malaria in Hawaii. Molecular Ecology 9, 1803–1814.CrossRefGoogle ScholarPubMed
Gomes, B., Sousa, C.A., Novo, M.T., Freitas, F.B., Alves, R., Côrte-Real, A.R., Salgueiro, P., Donnelly, M.J., Almeida, A.P.G. & Pinto, J. (2009) Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region, Portugal. BMC Evolutionary Biology 9, 262.CrossRefGoogle ScholarPubMed
Gutsevich, A.V., Monchadskii, A.S. & Shtakel'berg, A.A. (1974) Fauna of the USSR Diptera. Vol. 3, No. 4. Mosquitoes family Culicidae. Jerusalem, Keter Publishing House Jerusalem Ltd.Google Scholar
Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronic 4(1), 9. Available online at http://palaeo-electronica.org/2001_1/past/issue1_01.htm Google Scholar
Harbach, R.E., Harrison, B.A. & Gad, A.M. (1984) Culex (Culex) molestus Forskål (Diptera: Culicidae): neotype, designation, description, variation, and taxonomic status. Proceedings of the Entomological Society of Washington 86, 521–542.Google Scholar
Henry, A., Thongsripong, P., Fonseca-Gonzalez, I., Jaramillo-Ocampo, N. & Dujardin, J.P. (2010) Wing shape of dengue vectors from around the world. Infection, Genetics and Evolution 10, 207–214. Available online at http://www.biocidi.org.rs/ http://www.ecdc.europa.eu/en/healthtopics/west_nile_fever/West-Nile-fever-maps/Pages/index.aspx Google Scholar
Hubalek, Z. & Halouzka, J. (1999) West Nile fever-a reemerging mosquito-borne viral disease in Europe. Emerging Infectious Diseases 5, 643–650.Google Scholar
Jirakanjanakit, N., Leemingsawat, S., Thongrungkiat, S., Apiwathnasorn, C., Singhaniyom, S., Bellec, C. & Dujardin, J.P. (2007) Influence of larval density or food variation on the geometry of the wing of Aedes (Stegomyia) aegypti . Tropical Medicine and International Health 12, 1354–1360.Google Scholar
Jirakanjanakit, N., Leemingsawat, S. & Dujardin, J.P. (2008) The geometry of the wing of Aedes (Stegomyia) aegypti in isofemale lines through successive generations. Infection, Genetics and Evolution 8, 414–421.Google Scholar
Kemenesi, G. Krtinić, B., Milankov, V., Kutas, A., Dallos, B., Oldal, M., Somogyi, N., Nemeth, V., Banyai, K. & Jakab, F. (2014) West Nile virus surveillance in mosquitoes, April to October 2013, Vojvodina province, Serbia: implications for the 2014 season. Euro Surveillance 19(16), pii = 20779.Google ScholarPubMed
Kilpatrick, A.M., Meola, M.A., Moudy, R.M. & Kramer, L.D. (2008) Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathogens 4(6), e1000092.Google Scholar
Krtinić, B., Ludoški, J. & Milankov, V. (2012) Study on siphonal measurements and usefulness in delimitation of “rural” and “urban” ecotypes of Culex pipiens (Diptera, Culicidae). Bulletin of Insectology 65(1), 23–27.Google Scholar
Latrofa, M.S., Montarsi, F., Ciocchetta, S., Annoscia, G., Dantas-Torres, F., Ravagnan, S., Capelli, G. & Otranto, D. (2012) Molecular xenomonitoring of Dirofilaria immitis and Dirofilaria repens in mosquitoes from north-eastern Italy by real-time PCR coupled with melting curve analysis. Parasites and Vectors 5(1), 76.Google Scholar
Loetti, V., Schweigmanna, N. & Burronia, N. (2011) Development rates, larval survivorship and wing length of Culex pipiens (Diptera: Culicidae) at constant temperatures. Journal of Natural History 45, 2207–2217.Google Scholar
Lorenz, C., Marques, T.C., Salum, M.A.-M. & Suesdek, L. (2012) Morphometrical diagnosis of the malaria vectors Anopheles cruzii, An. homunculus and An. bellator . Parasites and Vectors 5, 257.CrossRefGoogle Scholar
Lundstrom, J.O. (1999) Mosquito-borne viruses in Western Europe: a review. Journal of Vector Ecology 24, 1–39.Google Scholar
Magnusson, K., Mendes, A.M., Windbichler, N., Papathanos, P-A., Nolan, T., Rizzi, E., Christophides, G.K. & Crisanti, A. (2011) Transcription regulation of sex-biased genes during ontogeny in the malaria vector Anopheles gambiae . PLoS ONE 6(6), e21572. doi: 10.1371/journal.pone.0021572.Google Scholar
Manimegalai, K., Arunachalam, M. & Udayakumari, R. (2009) Morphometric geometric study of wing shape in Culex quinquefasciatus Say (Diptera: Culicidae) from Tamil Nadu, India. Journal of Threatened Taxa 1(5), 263–268.Google Scholar
Marcus, L.E., Corti, M., Loy, A., Naylor, G.J.P. & Slice, D.E. (1996) Advances in Morphometrics. New York, Plenum.Google Scholar
Marshall, F. (1938) The British Mosquitoes. British Museum (Natural History). London, pp. 341.Google Scholar
McCann, S., Day, J.F., Allan, S. & Lord, C.C. (2009) Age modifies the effect of body size on fecundity in Culex quinquefasciatus Say (Diptera: Culicidae). Journal of Vector Ecology 34(2), 174–181.Google Scholar
Miles, S.J. & Paterson, H.E. (1979) Protein variation and systematics in the Culex pipiens group of species. Mosquito Systematics 11, 187–202.Google Scholar
Morais, S.A., Moratore, C., Suesdek, L. & Marrelli, M. (2010) Genetic morphometric variation in Culex quinquefasciatus from Brazil and La Plata, Argentina. Memorias do Instituto Oswaldo Cruz 105, 672–676.Google Scholar
Morales-Vargas, E.R., Ya-Umphan, P., Phumala-Morales, N., Komalamisra, N. & Dujardin, J.P. (2010) Climate associated size and shape changes in Aedes aegypti (Diptera: Culicidae) populations from Thailand. Infection, Genetics and Evolution 10, 580–585.Google Scholar
Motoki, M.T., Suesdek, L., Sterlino Bergo, E. & Salum, M.A-M. (2012) Wing geometry of Anopheles darlingi Root (Diptera: Culicidae) in five major Brazilian ecoregions. Infection, Genetics and Evolution 12, 1246–1252.CrossRefGoogle ScholarPubMed
Osório, H.C., Zé-Zé, , Amaro, F., Nunes, A. & Alves, M.J. (2014) Sympatric occurrence of Culex pipiens (Diptera, Culicidae) biotypes pipiens, molestus and their hybrids in Portugal, Western Europe: feeding patterns and habitat determinants. Medical and Veterinary Entomology 28, 103–109.Google Scholar
Petric, D., Hrnjakovic Cvjetkovic, I., Radovanov, J., Cvjetkovic, D., Jerant Patic, V., Milosevic, V., Kovacevic, G., Zgomba, M., Ignjatovic Cupina, A., Konjevic, A., Marinkovic, D. & Sánchez-Seco, M.P. (2012) West nile virus surveillance in humans and mosquitoes and detection of cell fusing agent virus in Vojvodina province (Serbia). HealthMED 6(2), 462–468.Google Scholar
Pradier, S., Lecollinet, S. & Leblond, A. (2012) West Nile virus epidemiology and factors triggering change in its distribution in Europe. Revue scientifique et technique (International Office of Epizootics) 31(3), 829–844.Google Scholar
Richards, S.L., Lord, C.C., Pesko, K.A. & Tabachnick, W.J. (2009) Environmental and biological factors influence Culex pipiens quinquefasciatus Say (Diptera: Culicidae) vector competence for Saint Louis encephalitis virus. American Journal of Tropical Medicine and Hygiene 81, 264–272.Google Scholar
Rohlf, F.J. (2010) tpsRelw, version 1.49. Department of Ecology and Evolution, State University of New York at Stony Brook. New York, NY. Available online at http://life.bio.sunysb.edu/morph/index.html.Google Scholar
Rohlf, F.J. (2011) tpsRegr, version 1.38. Department of Ecology and Evolution, 608 State University of New York at Stony Brook. New York, NY. Available online at http://life.bio.sunysb.edu/morph/index.html.Google Scholar
Rohlf, F.J. (2013) tpsDig, version 2.17. Department of Ecology and Evolution, State University of New York at Stony Brook. New York, NY. Available online at http://life.bio.sunysb.edu/morph/index.html.Google Scholar
Rohlf, F.J. & Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology and Evolution 8, 129–132.Google Scholar
Rohlf, F.J. & Slice, D. (1990) Extensions of the Procustes method for the optimal superimposition of landmarks. Systematic Zoology 39, 40–59.Google Scholar
Rohlf, F.J., Loy, A. & Corti, M. (1996) Morphometric analysis of old world Talpidae (Mammalia, Insectivora) using partial-warp scores. Systematic Biology 45, 344–362.Google Scholar
Schneider, J.R., Chadee, D.D., Mori, A., Romero-Severson, J. & Severson, D.W. (2011) Heritability and adaptive phenotypic plasticity of adult body size in the mosquito Aedes aegypti with implications for dengue vector competence. Infection, Genetics and Evolution 11, 11–16.CrossRefGoogle ScholarPubMed
StatSoft Inc . (2012) STATISTICA, (data analysis software system) version 10. Available online at www.statsoft.com.Google Scholar
Stillwell, R.C., Blanckenhorn, W.U., Teder, T., Davidowitz, G. & Fox, C.W. (2010) Sex differences in phenotypic plasticity of body size affect variation in sexual size dimorphism in insects: from physiology to evolution. Annual Review of Entomology 55, 227–245.Google Scholar
Vicente, J.L., Sousa, C.A., Alten, B., Caglar, S.S., Falcutá, E., Latorre, J.M., Toty, C., Barré, H., Demirci, B., Di Luca, M., Toma, L., Alves, R., Salgueiro, P., Silva, T.L., Bargues, M.D., Mas-Coma, S., Boccolini, D., Romi, R., Nicolescu, G., do Rosário, V.E., Ozer, N., Fontenille, D. & Pinto, J. (2011) Genetic and phenotypic variation of the malaria vector Anopheles atroparvus in southern Europe. Malaria Journal 10, 5.Google Scholar
Vidal, P.O., Peruzin, M.C. & Suesdek, L. (2011) Wing diagnostic characters for Culex quinquefasciatus and Culex nigripalpus (Diptera: Culicidae). Revista Brasielirade Entomologia 55, 134–137.Google Scholar
Vidal, P.O., Carvalho, E. & Suesdek, L. (2012) Temporal variation of wing geometry in Aedes albopictus . Memorias do Instituto Oswaldo Cruz 107(8), 1030–1034.Google Scholar
Vinogradova, E.B. (2000) Culex Pipiens Pipiens Mosquitoes: Taxonomy, Distribution, Ecology, Physiology, Genetics, Applied Importance and Control. Moscow, Russia, Pensoft.Google Scholar
Vinogradova, E.B. (2003) Ecophysiological and morphological variations in mosquitoes of the Culex pipiens complex (Diptera: Culicidae). Acta Societatis Zoologicae Bohemicae 67, 41–50.Google Scholar
Vinogradova, E.B. & Ivnitsky, S.B. (2009) Variability of quantitative morphological traits of mosquito larvae in some species of the Culex pipiens complex (Diptera: Culicidae). Entomological Revue 4, 390–398.CrossRefGoogle Scholar
Vinogradova, E.B., Reznik, S.Y. & Kuprijanova, E.S. (1996) Ecological and geographical variations in the siphonal index of Culex pipiens larvae (Diptera: Culicidae). Bulletin of Entomological Research 86, 281–287.Google Scholar
Vujić, A., Stefanović, A., Dragićević, I., Matijević, T., Pejčić, L., Knezević, M., Krasić, D. & Veselić, S. (2010) Species composition and seasonal dynamics of mosquitoes (Diptera: Culicidae) in flooded areas of Vojvodina, Serbia. Archives of Biological Science 62(4), 1193–1206.CrossRefGoogle Scholar
Weitzel, T., Collado, A., Jöst, A., Pietsch, K., Storch, V. & Becker, N. (2009) Genetic differentiation of populations within the Culex pipiens complex and phylogeny of related species. Journal of American Mosquito Control Association 25(1), 6–17.Google Scholar
Zelditch, M.L., Swiderski, D.L., Sheets, H.D. & Fink, W.L. (2004) Geometric Morphometrics for Biologists: A Primer. London, Elsevier Academic Presss.Google Scholar
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