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Morphological, biometrical and molecular characterization of Archaeopsylla erinacei (Bouché, 1835)

Published online by Cambridge University Press:  22 December 2017

A. Zurita ,
R. Callejón ,
M. de Rojas  and
C. Cutillas
A. Zurita
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
R. Callejón
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
M. de Rojas
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
C. Cutillas*
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
*
*Author for correspondence Phone: +34954556773 Fax: +34 954 628162 E-mail: cutillas@us.es
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Abstract

In the present work, we carried out a morphological, biometrical and molecular study of the species Archaeopsylla erinacei (Bouché, 1835) and their subspecies: Archaeopsylla erinacei erinacei (Bouché, 1835) and Archaeopsylla erinacei maura (Jordan & Rothschild, 1912) isolated from hedgehogs (Erinaceus europaeus) from different geographical regions (Seville and Corse). We have found morphological differences in females of A. erinacei from the same geographical origin that did not correspond with molecular differences. We suggest that some morphological characters traditionally used to discriminate females of both subspecies should be revised as well as we set the total length of the spermatheca as a valid criterion in order to discriminate between both subspecies. The Internal Transcribed Spacers 1 and 2 (ITS1, ITS2) and partial 18S rRNA gene, and partial cytochrome c-oxidase 1 (cox1) and cytochrome b (cytb) mtDNA gene sequences were determined to clarify the taxonomic status of these taxa and to assess intra-specific and intra-population similarity. In addition, a phylogenetic analysis with other species of fleas using Bayesian and Maximum Likelihood analysis was performed. All molecular markers used, except 18S, showed molecular differences between populations corresponding with geographical origins. Thus, based on the phylogenetic and molecular study of two nuclear markers (ITS1, ITS2) and two mitochondrial markers (cox1 and cytb), as well as concatenated sequences of both subspecies, we reported the existence of two geographical genetic lineages in A. erinacei corresponding with two different subspecies: A. e. erinacei (Corse, France) and A. e. maura (Seville, Spain), that could be discriminated by polymerase chain reaction-linked random-fragment-length polymorphism.

Keywords

Archaeopsylla erinaceimorphologymolecular studyribosomal DNAmitochondrial DNA

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Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 6 , December 2018 , pp. 726 - 738
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Copyright © Cambridge University Press 2017 

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References

Beaucournu, J.C. & Gomez-Lopez, M.S. (2015) Orden Siphonaptera. Revista IDE@ – SEA 61A, 1–11.Google Scholar
Beaucournu, J.C. & Launay, H. (1990) Les Puces (Siphonaptera) de France et du Bassin méditerranéen occidental. Paris, Faune de France, 76, Fedération Française des Sociétés des Sciences Naturelles.Google Scholar
Bouché, P.F. (1835) Beiträge zur Insektenkunde. II. Bemerkungen über die Gattung Pulex. Nova Acta Physico Medica 17, 493–508.Google Scholar
Brinkerhoff, R.J., Martin, A.P., Jones, R.T. & Collinge, S.K. (2011) Population genetic structure of the prairie dog flea and plague vector, Oropsylla hirsuta. Parasitology 138, 71–79.Google Scholar
Carew, M.E., Pettigrove, V., Cox, R.L. & Hoffmann, A.A. (2007) DNA identification of urban Tanytarsini chironomids (Diptera: Chironomidae). Journal of the North American Benthological Society 26, 587–600.Google Scholar
Cutillas, C., Callejón, R., de Rojas, M., Tewes, B., Ubeda, J.M., Ariza, C. & Guevara, D.C. (2009) Trichuris suis and Trichuris trichiura are different nematode species. Acta Tropica 111, 299–307.Google Scholar
Dittmar, K. & Whiting, M.F. (2003) Genetic and phylogeographic structure of populations of Pulex simulans (Siphonaptera) in Peru inferred from two genes (CytB and CoII). Journal of Parasitolology Research 91, 55–59.Google Scholar
Domínguez, G. (2004) North Spain (Burgos) wild mammals ectoparasites. Parasite 11, 267–272.Google Scholar
Dunnet, G.M. & Mardon, D.K. (1991) Siphonaptera. pp. 125–140 in Naumann, P.B.C.I.D., Lawrence, J.F., Nielsen, E.S., Spradberry, J.P., Taylor, R.W., Whitten, M.J. & Littlejohn, M.J. (Eds) Siphonaptera. Melbourne, CSIRO and Melbourne Univ. Press.Google Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.Google Scholar
Gamerschlag, S., Mehlhorn, H., Heukelbach, J., Feldmeier, H. & D'Haese, J. (2008) Repetitive sequences in the ITS1 region of the ribosomal DNA of Tunga penetrans and other flea species (Insecta, Siphonaptera). Parasitology Research 102, 193–199.Google Scholar
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & De Waard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London 270, 313–321.Google Scholar
Hopkins, G.H.E. & Rothschild, M. (1953) An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History). Vol. 1. Tungidae and Pulicidae. London, Trustees of the British Museum (Natural History).Google Scholar
Huelsenbeck, J.P. & Rannala, B. (1997) Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276, 227–232.Google Scholar
Jordan, K. & Rothschild, N.C. (1912) On Siphonaptera collected in Algeria. Novitates Zoologicae 19, 357–372.Google Scholar
Kaewmongkol, G., Kaewmongkol, S., Mclnnes, L.M., Burmej, H., Bennet, M.D., Adams, P.J., Ryan, U., Irwin, P.J. & Fenwick, S.G. (2011) Genetic characterization of flea derived Bartonella species from native animals in Australia suggest host-parasite co-evolution. Infection, Genetics and Evolution 11, 1868–1872.Google Scholar
Kramer, F. & Mencke, N. (2001) Flea Biology and Control. Berlin, Heidelberg, New York, Ed. Springer-Verlag, pp. 5–7.Google Scholar
Krasnov, B.R. (2008) Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge, UK, New York, Cambridge University Press.Google Scholar
Lane, R.P. & Crosskey, R.W. (1993) Medical Insects and Arachnids. London, UK, Ed. Chapman & Hall, pp. 529–575.Google Scholar
Lawrence, A., Hii, S.F., Jirsová, D., Panáková, L., Ionica, A.M., Gilchrist, K., Modrý, D., Mihalca, A., Webb, C.E., Traub, R.J. & Slapeta, J. (2015) Integrated morphological and molecular identification of cat fleas (Ctenocephalides felis) and dog fleas (Ctenocephalides canis) vectoring Rickettsia felis in central Europe. Veterinary Parasitology 210, 215–223.Google Scholar
Lawrence, A.L., Brown, G.K., Peters, B., Spielman, D.S., Morin-Adeline, M. & Slapeta, J. (2014) High phylogenetic diversity of the cat flea (Ctenocephalides felis) at two mitochondrial DNA markers. Medical and Veterinary Entomology 28, 330–336.Google Scholar
Lewis, R.E. (1967) Contributions to a taxonomic revision of the genus Nosopsyllus Jordan, 1933. Journal of Medical Entomology 4, 123–142.Google Scholar
Lewis, R.E. (1993) Notes on the geographical distribution and host preferences in the order Siphonaptera. Part 8. New taxa described between 1984 and 1990, with a current classification of the order. Journal of Medical Entomology 30, 239–256.Google Scholar
Lewis, R.E. (1998) Resume of the Siphonaptera (Insecta) of the world. Journal of Medical Entomology 35, 377–389.Google Scholar
Linardi, P.M. & Santos, J.L.C. (2012) Ctenocephalides felis felis vs Ctenocephalides canis (Siphonaptera:Pulicidae): some issues incorrectly identify these species. Brazilian Journal of Veterinary Parasitology 4, 345–354.Google Scholar
Losos, J.B. & Ricklefs, R.E. (2009) Adaptation and diversification on islands. Nature 457, 830–836.Google Scholar
Luchetti, A., Trentini, M., Pampiglone, S., Fiorawanti, M.L. & Mantovani, B. (2007) Genetic variability of Tunga penetrans (Siphonaptera, Tungidae) and fleas across South America and Africa. Journal of Parasitolology Research 100, 593–598.Google Scholar
Marrugal, A., Callejón, R., de Rojas, M., Halajian, A. & Cutillas, C. (2013) Morphological, biometrical and molecular characterization of Ctenocephalides felis and Ctenocephalides canis isolated from dogs from different geographical regions. Parasitology Research 112, 2289–2298.Google Scholar
Medvedev, S., Lobanov, A. & Lyangouzov, I. (2005) World database of fleas (Parhost). Available online at http://www.zin.ru/Animalia/Siphonaptera.Google Scholar
Mehlhorn, H. (2001) Encyclopaedic References of Parasitology. Berlin, Springer-Verlag.Google Scholar
Pardo, A. & Ruiz, M.A. (2002) SPSS 11. Guía para el análisis de datos. Madrid, McGraw-Hill.Google Scholar
Posada, D. (2008) Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Posada, D. & Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.Google Scholar
Rambaut, A. & Drummond, A. (2007) Tracer v1.6. Available online at http://beast.bio.ed.ac.uk/.Google Scholar
Ricklefs, R.E. & Bermingham, E. (2001) Nonequilibrium diversity dynamics of the lesser A ntillean avifauna. Science 294, 1522–1524.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Stothard, P. (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28, 1102–1104.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Traub, R. & Starcke, H. (1980) Fleas: Proceedings of the International Conference on Fleas. Rotterdam, A. A. Balkema.Google Scholar
Van der Mescht, L., Matthee, S. & Matthee, C.A. (2015) Comparative phylogeography between two generalist flea species reveal a complex interaction between parasite life history and host vicariance: parasite-host association matters. BMC Evolutionary Biology 15, 105. doi: 10.1186/s12862-015-0389-y.Google Scholar
Vobis, M., D'Haese, J., Mehlhorn, H., Mencke, N., Blagburn, B.L., Bond, R., Denholm, I., Dryden, M.W., Payne, P., Rust, M.K., Schroeder, I., Vaughn, M.B. & Bledsoe, D. (2004) Molecular phylogeny of isolates of Ctenocephalides felis and related species based on analysis of ITS1, ITS2 and mitochondrial 16S rDNA sequences and random binding primers. Parasitology Research 94, 219–226.Google Scholar
Whiting, M.F. (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104.Google Scholar
Whiting, M.F., Whiting, A.S., Hastriter, M.W. & Dittmar, K. (2008) A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24, 677–707.Google Scholar
Zhu, Q., Hastriter, M.W., Whiting, M.F. & Dittmar, K. (2015) Fleas (Siphonaptera) are Cretaceous, and evolved with Theria. Molecular Phylogenetics and Evolution 90, 129–139.Google Scholar
Zurita, A., Callejón, R., De Rojas, M., Gómez-López, M.S. & Cutillas, C. (2015) Molecular study of Stenoponia tripectinata tripectinata (Siphonaptera: Ctenophthalmidae: Stenoponiinae) from the Canary Islands: taxonomy and phylogeny. Bulletin of Entomological Research 104, 704–711.Google Scholar
Zurita, A., Callejón, R., De Rojas, M., Halajian, A. & Cutillas, C. (2016) Ctenocephalides felis and Ctenocephalides canis: introgressive hybridization? Systematic Entomology 41, 567–579.Google Scholar
Zurita, A., Callejón, R., De Rojas, M. & Cutillas, C. (2018) Morphological and molecular study of the genus Nosopsyllus (Siphonaptera: Ceratophyllidae). Nosopsyllus barbarus (Jordan & Rothschild 1912) as a junior synonym of Nosopsyllus fasciatus (Bosc, d'Antic 1800). Insect Systematic and Evolution 49, 81–101.Google Scholar
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