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Population structure of Cicada barbara Stål (Hemiptera, Cicadoidea) from the Iberian Peninsula and Morocco based on mitochondrial DNA analysis

  • G.A. Pinto-Juma (a1) (a2), J.A. Quartau (a1) and M.W. Bruford (a2)

Abstract

We assess the genetic history and population structure of Cicada barbara in Morocco and the Iberian Peninsula, based on analysis of the mitochondrial cytochrome b gene. The divergence between Morocco and the Iberian Peninsula populations was strongly corroborated by the molecular data, suggesting genetically isolated populations with a low level of gene flow. The Ceuta population from Spanish North Africa was more similar to the Iberian populations than the surrounding Moroccan populations, suggesting that the Strait of Gibraltar has not been acting as a strict barrier to dispersal while the Rif Mountains have. The Iberian Peninsula specimens showed a signature of demographic expansion before that which occurred in Morocco, but some of the assumptions related to the demographic parameters should be considered with caution due to the small genetic variation found. The high haplotype diversity found in Morocco implies higher demographic stability than in the Iberian Peninsula populations. These results do not, however, suggest a Moroccan origin for Iberian cicadas; but the most northwest region in Africa, such as Ceuta, might have acted as a southern refuge for Iberian cicadas during the most severe climatic conditions, from where they could expand north when climate improved. The separation of two subspecies within C. barbara (C. barbara lusitanica and C. barbara barbara) finds support with these results.

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*Author for correspondence Fax: +44 (0)2920874305 E-mail: jumag@cf.ac.uk

References

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Albert, E.M., Zardoya, R. & García-París, M. (2007) Phylogeographical and speciation patterns in subterranean worm lizards of the genus Blanus (Amphisbaenia: Blanidae). Molecular Ecology 16, 15191531.
Arensburger, P., Simon, C. & Holsinger, K.E. (2004) Evolution and phylogeny of the New Zealand cicada genus Kikihia Dugdale (Homoptera: Auchenorryncha: Cicadidae) with special reference to the origin of the Kermadec and Norfolk Islands' species. Journal of Biogeography 31, 17691783.
Besnard, G., Khadari, B., Baradat, P. & Bervillé, A. (2002a) Olea europaea (Oleaceae) phylogeography based on chloroplast DNA polymorphism. Theoretical and Applied Genetics 104, 13531361.
Besnard, G., Khadari, B., Baradat, P. & Bervillé, A. (2002b) Combination of chloroplast and mitochondrial DNA polymorphisms to study cytoplasm genetic differentiation in the olive complex (Olea europaea L.). Theoretical and Applied Genetics 105, 139144.
Boulard, M. (1982) Les cigales du Portugal, contribution à leur étude (Homoptera, Cicadidae). Annales de la Société Entomologique de France 18, 181198.
Boulard, M. & Mondon, B. (1996) Vies et mémoires de cigales. Equinoxe, Barbentane.
Burban, C. & Petit, R.J. (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Molecular Ecology 12, 14871495.
Carranza, S., Arnold, E.N. & Pleguezuelos, J.M. (2006) Phylogeny, biogeography, and evolution of two Mediterranean snakes, Malpolon monspessulanus and Hemorrhois hippocrepis (Squamata, Colubridae), using mtDNA sequences. Molecular Phylogenetics and Evolution 40, 532546.
Caterino, M.S., Cho, S. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: a thriving tower of Babel. Annual Review of Entomology 45, 154.
Collina-Girard, J. (2001) L'Atlantide devant le détroit de Gibraltar? Mythe et géologie. Sciences de la Terre et des Planètes 333, 233240.
Cosson, J.-F., Hutterer, R., Libois, R., Sarà, M., Taberlet, P. & Vogel, P. (2005) Phylogeographical footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew, Crocidura russula (Mammalia: Soridae). Molecular Ecology 14, 11511162.
Cox, C.B. & Moore, P.D. (2005) Biogeography: An Ecological and Evolutionary Approach. 7th edn. 428 pp. Oxford, UK, Blackwell Publishing.
Davies, J.I. & Nixon, K.C. (1992) Populations, genetic variation and the delimitation of phylogenetic species. Systematic Biology 41, 421435.
Drotz, M.K. (2003) Speciation and mitochondrial DNA diversification of the diving beetles Agabus bipustulatus and A. wollastoni (Coleoptera, Dytiscidae) within Macaronesia. Biological Journal of the Linnean Society 79, 653666.
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.
Fritz, U., Barata, M., Busack, S.D., Fritzsch, G. & Castilho, R. (2005) Impact of mountain chains, sea straits and peripheral populations on genetic and taxonomic structure of a freshwater turtle, Mauremys leprosa (Reptilia, Testudines, Geoemydidae). Zoologica Scripta 35, 97108.
Fu, Y. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147, 915925.
Fu, Y. & Li, W.H. (1993) Statistical tests of neutrality of mutations. Genetics 133, 693709.
Giralda, A.A., Rodriguez, J.M.P. & Pintor, F.G. (1998) La cigarra del olivo o Magrebí-Cicada barbara (Stal.). Junta de Extremadura. Boletin Fitosanitario de Avisos e Informaciones 1/98, 14.
Gómez, A., Vendramin, G.G., González-Martínez, S.C. & Alía, R. (2005) Genetic diversity and differentiation of two Mediterranean pines (Pinus halepensis Mill. and Pinus pinaster Ait.) along a latitudinal cline using chloroplast microsatellite markers. Diversity and Distributions 11, 257263.
Harpending, H. (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591600.
Hasegawa, M., Kishino, K. & Yano, T. (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160174.
Hewitt, G.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58, 247276.
Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68, 87112.
Hewitt, G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907913.
Hewitt, G.M. (2001) Speciation, hybrid zones and phylogeography – or seen genes in space and time. Molecular Ecology 10, 537549.
Hewitt, G.M. (2004a) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 359, 183195.
Hewitt, G.M. (2004b) The structure of biodiversity – insights from molecular phylogeography. Frontiers in Zoology 1, 116.
Hooghiemstra, H., Stalling, H., Agwu, C.O.C. & Dupont, L.M. (1992) Vegetational and climatic changes at the northern fringe of the Sahara 250,000–5,000 years BP: evidence from 4 marine pollen records located between Portugal and the Canary Islands. Review of Palaeobotany and Palynology 74, 153.
Horn, A., Roux-Morabito, G., Lieutier, F. & Kerdelhue, C. (2006) Phylogeographic structure and past history of the circum-Mediterranean species Tomicus destruens Woll. (Coleoptera: Scolytinae). Molecular Ecology 15, 16031615.
Hsü, K.J., Montadert, L., Bernoulli, D., Bianca, C.M., Erickson, A., Garrison, R.E., Kidd, R.B., Mèliéres, F., Müller, C. & Wright, R. (1977) History of the Mediterranean salinity crisis. Nature 267, 399403.
Hughes, P.D., Woodward, J.C. & Gibbard, P.L. (2006) Quaternary glacial history of the Mediterranean mountains. Progress in Physical Geography 30, 334364.
Jansson, R. & Dynesius, M. (2002) The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annual Review of Ecology and Systematics 33, 741777.
Krzywinski, J., Wilkerson, R.C. & Besansky, N.J. (2001) Evolution of mitochondrial and ribosomal gene sequences in Anophelinae (Diptera: Culicidae): implications for phylogeny reconstruction. Molecular Phylogenetics and Evolution 18, 479487.
Kumar, S., Tamura, K., Jakobsen, I.B. & Nei, M. (2001) MEGA2: Molecular Evolutionary Genetics Analysis software, Arizona State University, Tempe,, USA.
Lee, M.S.Y. (2004) The molecularisation of taxonomy. Invertebrate Systematics 18, 16.
Lindner, L., Dzierzek, J., Marciniak, B. & Nitychoruk, J. (2003) Outline of Quaternary glaciations in the Tatra Mts.: their development, age and limits. Geological Quarterly 47, 269280.
Mes, T.H.M. (2003) Demographic expansion of parasitic nematodes of livestock based on mitochondrial DNA regions that conflict with the infinite-sites model. Molecular Ecology 12, 15551566.
Modolo, L., Salzburger, W. & Martin, R.D. (2005) Phylogeography of Barbary macaques (Macaca sylvanus) and the origin of the Gibraltar colony. The Proceedings of the National Academy of Sciences Online 102, 73927397.
Monteiro, F.A., Donnelly, M.J., Beard, C.B. & Costa, J. (2004) Nested clade and phylogeographic analyses of the chagas disease vector Triatoma brasiliensis in northeast Brazil. Molecular Phylogenetics and Evolution 32, 4656.
Moore, H.M., Fox, H.R., Harrouni, M.C. & El Alami, A. (1998) Environmental challenges in the Rif mountains, northern Morocco. Environmental Conservation 25, 354365.
Ortiz, M.Á., Tremetsberger, K., Talavera, S., Stuessy, T. & García-Castaño, J.L. (2007) Population structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the Strait of Gibraltar, in relation to Quaternary sea level changes. Molecular Ecology 16, 541552.
Palmer, M. & Cambefort, Y. (2000) Evidence for reticulate palaeogeography: beetle diversity linked to connection-disjunction cycles of the Gibraltar strait. Journal of Biogeography 27, 403416.
Paulo, O.S., Dias, C., Bruford, M.W., Jordan, W.C. & Nichols, R.A. (2001) The persistence of Pliocene populations through the Pleistocene climatic cycles: evidence from the phylogeography of an Iberian lizard. Proceedings of the Royal Society of London. Series B: Biological Sciences 268, 16251630.
Phillimore, A.B. & Owens, I.P.F. (2006) Are subspecies useful in evolutionary and conservation biology? Proceedings of the Royal Society B: Biological Sciences 273, 10491053.
Pinho, C., Harris, D.J. & Ferrand, N. (2007) Contrasting patterns of population subdivision and historical demography in three western Mediterranean lizard species inferred from mitochondrial DNA variation. Molecular Ecology 16, 11911205.
Pinto, G.A., Quartau, J.A., Morgan, J.C. & Hemingway, J. (1998) Preliminary data on the sequencing of a fragment of cytochrome b gene of mitochondrial DNA in Cicada orni L. (Homoptera: Cicadidae) in Portugal. Boletim da Sociedade Portuguesa de Entomologia 7(6), 5766.
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics Applications Note 14, 817818.
Quartau, J.A. (1988) A numerical analysis of interspecific morphological differences in two closely related species of Cicada (Homoptera, Cicadoidea) in Portugal. Great Basin Naturalist Memoirs 12, 171181.
Quartau, J.A. (1995) Cigarras esses insectos quase desconhecidos. Correio da Natureza 19, 3338.
Quartau, J.A., Ribeiro, M., Simões, P.C. & Crespo, A. (2000) Taxonomic separation by isozyme electrophoresis of two closely related species of Cicada L. (Hemiptera: Cicadoidea) in Portugal. Journal of Natural History 34, 16771684.
Quartau, J.A., Ribeiro, M., Simões, P.C. & Coelho, M.M. (2001) Genetic divergence among populations of two closely related species of Cicada Linnaeus (Hemiptera: Cicadoidea) in Portugal. Insect Systematics and Evolution 32, 99106.
Ramos-Onsins, S. & Rozas, J. (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 20922100.
Rogers, A.R. (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49, 608615.
Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552569.
Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 24962497.
Sánchez Goñi, M.F., Turon, J.-L., Eynaud, F., Schackleton, N.J. & Cayre, O. (2000) Direct land/sea correlation of the Eemian and its comparison with the Holocene: a high-resolution palynological record of the Iberian Margin. Netherlands Journal of Geosciences 79, 345354.
Schmitt, T. (2007) Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology 4(11), 113.
Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin: A software for population genetics data analysis. Ver. 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva.
Simmons, R.B. & Weller, S.J. (2001) Utility and evolution of cytochrome b in insects. Molecular Phylogenetics and Evolution 20, 196210.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, 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.
Slatkin, M. (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457462.
Swofford, D.L. (1999) PAUP 4.0 beta version. Phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, Massachusetts.
Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G. & Cosson, J.-F. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453464.
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.
Templeton, A.R. (1994) The role of molecular genetics in speciation studies. pp. 455477in Schierwater, B., Streit, B., Wagner, G.P. & DeSalle, R. (Eds) Molecular Ecology and Evolution: Approaches and Applications. Basel, Switzerland, Birkhauser Verlag.
Yokoyama, Y., Lambeck, K., De Deckker, P., Johnston, P. & Fifield, L.K. (2000) Timing of the Last Glacial Maximum from observed sea-level minima. Nature 406, 713716.
Zink, R.M. (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society B: Biological Sciences 271, 561564.

Keywords

Population structure of Cicada barbara Stål (Hemiptera, Cicadoidea) from the Iberian Peninsula and Morocco based on mitochondrial DNA analysis

  • G.A. Pinto-Juma (a1) (a2), J.A. Quartau (a1) and M.W. Bruford (a2)

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