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

Published online by Cambridge University Press:  07 December 2007

G.A. Pinto-Juma ,
J.A. Quartau  and
M.W. Bruford
G.A. Pinto-Juma*
Affiliation:
Centro de Biologia Ambiental/Departamento de Biologia Animal, Faculdade de Ciências de Lisboa, C2, Campo Grande, 1749-016 Lisboa, Portugal School of Biosciences, Cardiff University, Cardiff CF10 3US, Wales, UK
J.A. Quartau
Affiliation:
Centro de Biologia Ambiental/Departamento de Biologia Animal, Faculdade de Ciências de Lisboa, C2, Campo Grande, 1749-016 Lisboa, Portugal
M.W. Bruford
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3US, Wales, UK
*
*Author for correspondence Fax: +44 (0)2920874305 E-mail: jumag@cf.ac.uk
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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.

Keywords

Cicada barbaraHemipteramitochondrial cytochrome bsubspeciesgenetic variationpopulation structuredemographic expansionsStrait of Gibraltar
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 1 , February 2008 , pp. 15 - 25
Copyright
Copyright © Cambridge University Press 2008

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References

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, 1519–1531.CrossRefGoogle ScholarPubMed
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, 1769–1783.CrossRefGoogle Scholar
Besnard, G., Khadari, B., Baradat, P. & Bervillé, A. (2002a) Olea europaea (Oleaceae) phylogeography based on chloroplast DNA polymorphism. Theoretical and Applied Genetics 104, 1353–1361.CrossRefGoogle ScholarPubMed
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, 139–144.CrossRefGoogle ScholarPubMed
Boulard, M. (1982) Les cigales du Portugal, contribution à leur étude (Homoptera, Cicadidae). Annales de la Société Entomologique de France 18, 181–198.CrossRefGoogle Scholar
Boulard, M. & Mondon, B. (1996) Vies et mémoires de cigales. Equinoxe, Barbentane.Google Scholar
Burban, C. & Petit, R.J. (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Molecular Ecology 12, 1487–1495.CrossRefGoogle ScholarPubMed
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, 532–546.CrossRefGoogle ScholarPubMed
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, 1–54.CrossRefGoogle ScholarPubMed
Collina-Girard, J. (2001) L'Atlantide devant le détroit de Gibraltar? Mythe et géologie. Sciences de la Terre et des Planètes 333, 233–240.Google Scholar
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, 1151–1162.CrossRefGoogle Scholar
Cox, C.B. & Moore, P.D. (2005) Biogeography: An Ecological and Evolutionary Approach. 7th edn. 428 pp. Oxford, UK, Blackwell Publishing.Google Scholar
Davies, J.I. & Nixon, K.C. (1992) Populations, genetic variation and the delimitation of phylogenetic species. Systematic Biology 41, 421–435.CrossRefGoogle Scholar
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, 653–666.CrossRefGoogle Scholar
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, 479–491.CrossRefGoogle ScholarPubMed
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, 97–108.CrossRefGoogle Scholar
Fu, Y. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Fu, Y. & Li, W.H. (1993) Statistical tests of neutrality of mutations. Genetics 133, 693–709.CrossRefGoogle ScholarPubMed
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, 1–4.Google Scholar
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, 257–263.CrossRefGoogle Scholar
Harpending, H. (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591–600.Google Scholar
Hasegawa, M., Kishino, K. & Yano, T. (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.CrossRefGoogle ScholarPubMed
Hewitt, G.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58, 247–276.CrossRefGoogle Scholar
Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68, 87–112.CrossRefGoogle Scholar
Hewitt, G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.CrossRefGoogle ScholarPubMed
Hewitt, G.M. (2001) Speciation, hybrid zones and phylogeography – or seen genes in space and time. Molecular Ecology 10, 537–549.CrossRefGoogle ScholarPubMed
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, 183–195.CrossRefGoogle ScholarPubMed
Hewitt, G.M. (2004b) The structure of biodiversity – insights from molecular phylogeography. Frontiers in Zoology 1, 1–16.CrossRefGoogle ScholarPubMed
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, 1–53.CrossRefGoogle Scholar
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, 1603–1615.CrossRefGoogle ScholarPubMed
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, 399–403.CrossRefGoogle Scholar
Hughes, P.D., Woodward, J.C. & Gibbard, P.L. (2006) Quaternary glacial history of the Mediterranean mountains. Progress in Physical Geography 30, 334–364.CrossRefGoogle Scholar
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, 741–777.CrossRefGoogle Scholar
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, 479–487.CrossRefGoogle ScholarPubMed
Kumar, S., Tamura, K., Jakobsen, I.B. & Nei, M. (2001) MEGA2: Molecular Evolutionary Genetics Analysis software, Arizona State University, Tempe,, USA.CrossRefGoogle Scholar
Lee, M.S.Y. (2004) The molecularisation of taxonomy. Invertebrate Systematics 18, 1–6.CrossRefGoogle Scholar
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, 269–280.Google Scholar
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, 1555–1566.CrossRefGoogle ScholarPubMed
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, 7392–7397.CrossRefGoogle ScholarPubMed
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, 46–56.CrossRefGoogle ScholarPubMed
Moore, H.M., Fox, H.R., Harrouni, M.C. & El Alami, A. (1998) Environmental challenges in the Rif mountains, northern Morocco. Environmental Conservation 25, 354–365.CrossRefGoogle Scholar
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, 541–552.CrossRefGoogle Scholar
Palmer, M. & Cambefort, Y. (2000) Evidence for reticulate palaeogeography: beetle diversity linked to connection-disjunction cycles of the Gibraltar strait. Journal of Biogeography 27, 403–416.CrossRefGoogle Scholar
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, 1625–1630.CrossRefGoogle ScholarPubMed
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, 1049–1053.CrossRefGoogle ScholarPubMed
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, 1191–1205.CrossRefGoogle ScholarPubMed
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), 57–66.Google Scholar
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics Applications Note 14, 817–818.Google ScholarPubMed
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, 171–181.Google Scholar
Quartau, J.A. (1995) Cigarras esses insectos quase desconhecidos. Correio da Natureza 19, 33–38.Google Scholar
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, 1677–1684.CrossRefGoogle Scholar
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, 99–106.Google Scholar
Ramos-Onsins, S. & Rozas, J. (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.CrossRefGoogle ScholarPubMed
Rogers, A.R. (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49, 608–615.CrossRefGoogle ScholarPubMed
Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.Google ScholarPubMed
Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefGoogle ScholarPubMed
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, 345–354.CrossRefGoogle Scholar
Schmitt, T. (2007) Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology 4(11), 1–13.CrossRefGoogle ScholarPubMed
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.Google Scholar
Simmons, R.B. & Weller, S.J. (2001) Utility and evolution of cytochrome b in insects. Molecular Phylogenetics and Evolution 20, 196–210.CrossRefGoogle ScholarPubMed
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, 651–701.CrossRefGoogle Scholar
Slatkin, M. (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462.CrossRefGoogle ScholarPubMed
Swofford, D.L. (1999) PAUP 4.0 beta version. Phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G. & Cosson, J.-F. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453–464.CrossRefGoogle ScholarPubMed
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Templeton, A.R. (1994) The role of molecular genetics in speciation studies. pp. 455–477in Schierwater, B., Streit, B., Wagner, G.P. & DeSalle, R. (Eds) Molecular Ecology and Evolution: Approaches and Applications. Basel, Switzerland, Birkhauser Verlag.CrossRefGoogle Scholar
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, 713–716.CrossRefGoogle ScholarPubMed
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, 561–564.CrossRefGoogle ScholarPubMed