Abstract
Fleas are holometabolous insects forming the order of Siphonaptera. Some studies have been carried out on biology and systematic of Malagasy fleas, but little is known about their phylogenetic relationships. In this study, we focused on flea species occurring in the forests of the Central Highlands and also, on the determination of their phylogenetic relationships. Three families, five genera and thirteen species were identified. The family Pulicidae includes four species (Centetipsylla madagascariensis Rothschild, Synopsyllus fonquerniei Wagner & Roubaud, S. estradei Klein and S. robici Klein); Leptopsyllidae has eight species (Paractenopsyllus vauceli Klein, P. petiti Klein, P. viettei Klein, P. grandidieri Klein, P. goodmani Duchemin, P. rouxi Duchemin, P. raxworthyi Duchemin & Ratovonjato and Tsaractenus rodhaini Duchemin), and Ctenophtalmidae one species (Dinopsyllus brachypecten Smit). All are endemic to Madagascar and each differs geographically. Flea phylogenetic relationships were inferred using four molecular markers (ITS2, mtCOII, 16SrRNA and 12S rRNA) and using Neighbor-Joining, Maximum Parsimony and Bayesian methods with addition of Genbank sequences of exotic species. The Family Pulicidae was monophyletic while the families Leptopsyllidae and Ctenophtalmidae were paraphyletic. Malagasy fleas are homogeneous and all species adhere to current classification schemes.
References
Beaucournu, J.-C. & Fontenille, D. (1993) Contribution à un catalogue des puces de Madagascar (Insecta, Siphonaptera). Archives de l'Institut Pasteur de Madagascar, 59, 57–98.
Beaucournu, J.-C., Randrenjarison, A.R.H. & Goodman, S.M. (2015) Puces (Insecta: Siphonaptera) d'Ambohitantely, Madagascar: Spécificité et phénologie. Malagasy Nature, 9, 39–48.
Brygoo, E.R. (1966) Epidemiologie de la peste à Madagascar. Archives de l'Institut Pasteur de Madagascar, 35, 9–147.
Cheetham, T.B. (1988) Male genitalia and the phylogeny of the Pulicoidea (Siphonaptera). Koeltz Scientific Books, Königstein, 244 pp.
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
https://doi.org/10.1038/nmeth.2109Duchemin, J.-B. (2003a) Biogéographie des puces de Madagascar. Faculté de Médecine de Créteil, Université de Paris XII, Paris, 254 pp.
Duchemin, J.-B. (2003b) Two new fleas (Siphonaptera: Ceratophyllidae: Leptopsyllinae) of Madagascar: Tsaractenus rodhaini n.sp. and Paractenopsyllus (Consobrinopsyllus n.subgen.) goodmani n.sp. Parasite, Paris, France, 10, 351–358.
https://doi.org/10.1051/parasite/2003104351Duchemin, J.-B. (2004) Leptopsyllines from Madagascar (Insecta: Siphonaptera: Ceratophyllidae): description of five new species of Paractenopsyllus Wagner, 1938. Parasite (Paris, France), 11, 59–70.
https://doi.org/10.1051/parasite/200411159Duchemin, J.-B. & Ratovonjato, J. (2004) Description de trois nouvelles espèces de Paractenopsyllus (Siphonaptera : Leptopsyllinae) de Madagascar. Parasites, 11, 253–260.
https://doi.org/10.1051/parasite/2004113253Dunnet, G.M. & Mardon, D.K. (1991) Siphonaptera. 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.), The Insects of Australia: a Textbook for Students and Research Workers. CSIRO and Melbourne University Press, Melbourne, pp. 125–140.
Duplantier, J.-M., Duchemin, J.-B., Chanteau, S. & Carniel, E. (2005) From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Veterinary Research, 36, 437–453.
https://doi.org/10.1051/vetres:2005007Duplantier, J.-M., Duchemin, J.B., Ratsitorahina, M., Rahalison, L. & Chanteau, S. (2001) Résurgence de la peste dans le district d'Ikongo à Madagascar en 1998. 2. Réservoirs et vecteurs impliqués. Bulletin de la Société de Pathologie Exotique, 94, 119–122.
Eads, D.A., Biggins, D.E., Doherty Jr, P.F., Gage, K.L., Huyvaert, K.P., Long, D.H., Gage, K.L., Huyvaert, K.P. & Antolin, M.F. (2013) Using occupancy models to investigate the prevalence of ectoparasitic vectors on hosts: An example with fleas on prairie dogs. International Journal for Parasitology: Parasites and Wildlife, 2, 246–256.
https://doi.org/10.1016/j.ijppaw.2013.09.002Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
https://doi.org/10.1093/nar/gkh340Girard, G. (1942) Le comportement de la puce Synopsyllus fonquerniei et son rôle dans la transmission de la peste. Bulletin de la Société de Pathologie Exotique, 35, 177–181.
Goodman, S.M., Ganzhorn, J.U. & Rakotondravony, D. (2003) Introduction to the mammals. In: Goodman, S.M. & Benstead, P. (Eds.), The natural history of Madagascar. The University of Chicago Press, Chicago, pp. 1159–1186.
Goodman, S.M., Randrenjarison, A.H.R., Soarimalala, V. & Beaucournu, J.-C. (2015) The fleas of endemic and introduced small mammals in Central Highland forests of Madagascar: Faunistics, species diversity, and absence of host specificity. Journal of Medical Entomology, 52, 1135–1143.
https://doi.org/10.1093/jme/tjv113Goodman, S.M., Raselimanana, A.P. & Wilmé, L. (2007) Inventaires de la faune et de la flore du couloir forestier d’Anjozorobe – Angavo. Vol. 24. Centre d'Information et de Documentation Scientifique et Technique, Antananarivo, 217 pp.
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
https://doi.org/10.1080/10635150390235520Hastriter, M.W. (2016) Description of two new species of bat fleas of the genus Araeopsylla (Siphonaptera) from Kenya and Madagascar with notes on miscellaneous bat fleas. ZooKeys, 572, 7–21.
https://doi.org/10.3897/zookeys.572.7823Hastriter, M.W. & Dick, C. (2009) A description of the flea species Paractenopsyllus madagascarensis n. sp. and the female sex of Paractenopsyllus raxworthyi Duchemin & Ratovonjato, 2004 (Siphonaptera, Leptopsyllidae) from Madagascar with a key to the species of Paractenopsyllus. ZooKeys, 13, 43–55.
https://doi.org/10.3897/zookeys.13.174Kambhampati, S. & Smith, P.T. (1995) PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Molecular Biology, 4, 233–236.
https://doi.org/10.1111/j.1365-2583.1995.tb00028.xKrasnov, B., Khokhlova, I. & Shenbrot, G. (2002) The effect of host density on ectoparasite distribution: An example of a rodent parasitized by fleas. Ecology, 83, 164–175.
https://doi.org/10.1890/0012-9658(2002)083[0164:TEOHDO]2.0.CO;2Laudisoit, A., Prié, V. & Beaucournu, J.-C. (2012) Une nouvelle espèce de Lagaropsylla Jordan & Rothschild, 1921 de Madagascar (Insecta, Siphonaptera, Ischnopsyllidae). Zoosystema, 34, 737–744.
https://doi.org/10.5252/z2012n4a5Lewis, R.E. & Lewis, J.H. (1985) Notes on the geographical distribution and host preferences in the order Siphonaptera. Journal of Medical Entomology, 22, 134–152.
https://doi.org/10.1093/jmedent/22.2.134Luchetti, A., Mantovani, B., Pampiglione, S. & Trentini, M. (2005) Molecular characterization of Tunga trimamillata and Tunga penetrans (Insecta, Siphonaptera, Tungidae): taxonomy and genetic variability. Parasite, 12, 123–129.
https://doi.org/10.1051/parasite/2005122123Lumaret, R. (1962) Faune de Madagascar: XV: Insectes Siphonaptères. Institut de Recherche Scientifique Madagascar, Antananarivo, 107 pp.
Ronquist, F., Huelsenbeck, J. & Teslenko, M. (2011) Draft MrBayes version 3.2 manual: tutorials and model summaries. 172 pp. Available from: http://mrbayes.sourceforge.net/mb3.2_manual.pdf (accessed 8 April 2015)
Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
St. Juliana, J.R., Khokhlova, I.S., Wielebnowski, N., Kotler, B.P. & Krasnov, B.R. (2014) Ectoparasitism and stress hormones: strategy of host exploitation, common host-parasite history and energetics matter. Journal of Animal Ecology, 83, 1113–1123.
https://doi.org/10.1111/1365-2656.12217Tamura, 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.
https://doi.org/10.1093/molbev/msr121Wagner, J. & Roubaud, E. (1932a) Sur un Pulicide nouveau, parasite des rats domestiques à Madagascar. Bulletin de la Société de Pathologie Exotique, 25, 327–332.
Wagner, J. & Roubaud, E. (1932b) Sur un Pulicide nouveau, parasite des rongeurs et insectivores de Madagascar. Bulletin de la Société de Pathologie Exotique, 25, 962–964.
Whiting, M.F. (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31, 93–104.
https://doi.org/10.1046/j.0300-3256.2001.00095.xWhiting, 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.
https://doi.org/10.1111/j.1096-0031.2008.00211.xWHO (2013) World Health Statistics. 168 pp. Available from: http://www.who.int/gho/publications/world_health_statistics/2013/en/ (accessed 30 July 2015)