Anales del Jardín Botánico de Madrid, Vol 68, No 2 (2011)

Genetic and morphological diversity in Armeria (Plumbaginaceae) is shaped by glacial cycles in Mediterranean refugia


https://doi.org/10.3989/ajbm.2260

Javier Fuertes Aguilar
Real Jardín Botánico, CSIC, Spain

Belén Gutiérrez Larena
Real Jardín Botánico, CSIC, Spain

Gonzalo Nieto Feliner
Real Jardín Botánico, CSIC, Spain

Abstract


Little is known of the direct effects of Quaternary glaciationdeglaciation cycles in plants within southern European refugia. This study, centered in the Sierra Nevada (S Spain), used RAPD and morphometric data from 36 populations of Armeria (Plumbaginaceae) from five taxa belonging to three species that are endemic to that region: A. filicaulis subsp. nevadensis, A. fili caulis subsp. trevenqueana, A. filicaulis subsp. alfacarensis, A. splendens, and A. villosa subsp. bernisii. The results based on genetic analyses at the population level (AMOVA, genetic diversity, genetic distance) and genetic and morphological analyses at individual level (haplotype phenetic distance, PCO, morphometrics) indicate that: (1) genetic diversity decreases with altitude, probably as a result of the postglacial recolonization processes, except in some secondary contact zones between taxa; (2) gene flow among interspecific populations, most likely facilitated by contraction of vegetation belts, led to the formation of hybrid taxa; (3) genetic distances among populations provide a useful basis for studying scenarios with frequent interspecific gene-flow since it allows distinguishing eventual cases of introgression from hybridogenous taxa.

Keywords


altitudinal gradient; glacial refugia; hybridization; Iberian Peninsula; phylogeography; reticulate evolution; Sierra Nevada

Full Text:


PDF

References


Aægisdóttir, H.H., Kuss & P., Stöcklin, J. 2009. Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Annals of Botany 104: 1313-1322. http://dx.doi.org/10.1093/aob/mcp242 PMid:19797423    PMCid:2778390

Abbott, R.J. & Comes, H. 2004. Evolution in the Arctic: a phylogeographic analysis of the circumarctic plant, Saxifraga oppositifolia (Purple saxifrage). New Phytologist. 161: 211-224. http://dx.doi.org/10.1046/j.1469-8137.2003.00953.x

Baker, H.G. 1966. The evolution, functioning and breakdown of heteromorphic incompatibility systems. I. The Plumbaginaceae. Evolution 20: 349-368. http://dx.doi.org/10.2307/2406635

Barrón, E., Rivas-Carballo, R., Postigo-Mijarra, J.M., Alcalde-Olivares, C., Vieira, M., Castro, L., Pais, J. & Valle-Hernández, M. 2010. The Cenozoic vegetation of the Iberian Peninsula: A synthesis. Review of Palaeobotany and Palynology 162: 382-402. http://dx.doi.org/10.1016/j.revpalbo.2009.11.007

Baumbach, H. & Hellwig, F.H. 2003. Genetic variation within and among metal-tolerant and non-tolerant populations of Armeria maritima (Mill.) Willd. s.l. (Plumbaginaceae) in Central and Northeast Germany. Plant Biology 5: 186-193. http://dx.doi.org/10.1055/s-2003-40729

Blanca, G., López Onieva, M.R., Lorite, J., Martínez Lirola, M.J., Molero Mesa, J., Quintas, S., Ruiz Girela, M., Varo, M.A. & Vidal, S. 2002. Flora amenazada y endémica de Sierra Nevada., Editorial Universidad de Granada. 407 pp.

Braga, J.C., Martín, J.M. & Quesada, C. 2003. Patterns and average rates of late Neogene-Recent uplift of the Betic Cordillera, SE Spain. Geomorphology 50: 3-26. http://dx.doi.org/10.1016/S0169-555X(02)00205-2

Brochmann, C., Nilsson, T. & Gabrielsen, T.M. 1996. A classic exam ple of postglacial allopolyploid speciation re-examined using RAPD markers and nucleotide sequences: Saxifraga osloensis (Saxifragaceae). Symbolae Botanicae Upsalienses 31: 75-89.

Brochmann, C., Xiang, Q.-Y., Brunsfeld, S.J., Soltis, D.E. & Soltis, P.S. 1998. Molecular evidence for polyploid origins in Saxifraga (Saxifragaceae): the narrow arctic endemic S. svalbardensis and its widespread allies. American Journal of Botany 85: 135-143. http://dx.doi.org/10.2307/2446562 PMid:21684887

Carrión, J.S. 2002. Patterns and processes of Late Quaternary environmental change in a montane region of southwestern Europe. Quaternary Science Reviews 21: 2047-2066. http://dx.doi.org/10.1016/S0277-3791(02)00010-0

Carrión, J.S., Munuera, M., Dupré, M. & Andrade, A. 2001a. Abrupt vegetation changes in the Segura Mountains of southern Spain throughout the Holocene. Journal of Ecology 89: 783-797. http://dx.doi.org/10.1046/j.0022-0477.2001.00601.x

Carrión, J.S., Riquelme, J. A., Navarro, C. & Munuera, M. 2001b. Pollen in hyaena coprolites reflects late glacial landscape in southern Spain. Palaeogeography, Palaeoclimatology, Palaeoecology 176: 193-205. http://dx.doi.org/10.1016/S0031-0182(01)00338-8

Carrión, J.S., Yll, E.I., Walker, M.J., Legaz, A.J., Chaín, C. & López, A. 2003. Glacial refugia of temperate, Mediterranean and Ibero-North African flora in south-eastern Spain: new evidence from cave pollen at two Neanderthal man sites. Global Ecology and Biogeography 12: 119-129. http://dx.doi.org/10.1046/j.1466-822X.2003.00013.x

Comes, H.P. & Kadereit, J.W. 1998. The effect of Quaternary climatic changes on plant distribution and evolution. Trends in Plant Science 3: 432-438. http://dx.doi.org/10.1016/S1360-1385(98)01327-2

Dice, L.R. 1945. Measures of the amount of ecologic association between species. Ecology 26: 297-302. http://dx.doi.org/10.2307/1932409

Doyle, J.J. & Doyle, J.L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11-15.

Evanno, G., Regnaut, S. & Goudet, J. 2005. Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology 14: 2611-2620. http://dx.doi.org/10.1111/j.1365-294X.2005.02553.x PMid:15969739

Falush, D., Stephens, M. & Pritchard, J.K. 2007.Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7: 574-578. http://dx.doi.org/10.1111/j.1471-8286.2007.01758.x PMid:18784791    PMCid:1974779

Ferris, C., King, R.A. & Hewitt, G.M. 1999. Isolation within species and the history of glacial refugia. In: Hollingsworth P.M., Bateman R.M. & Gornall, J. (eds.), Molecular systematics and plant evolution: 20-34. Taylor and Francis, London.

Fuertes Aguilar, J. & Nieto Feliner, G 2003. Additive polymorphisms and reticulation in an ITS phylogeny of thrifts (Armeria, Plumbaginaceae). Molecular Phylogenetics and Evolution 28: 430-447. http://dx.doi.org/10.1016/S1055-7903(02)00301-9

Fuertes Aguilar, J., Rosselló, J.A. & Nieto Feliner, G. 1999. Molecular evidence for the compilospecies model of reticulate evolution in Armeria (Plumbaginaceae). Systematic Biology 48: 735-754. http://dx.doi.org/10.1080/106351599259997

Gabrielsen, T. M., Bachmann, K., Jakobson, K.S. & Brochmann, C. 1997. Glacial survival does not matter: RAPD phylogeography of Nordic Saxifraga oppositifolia. Molecular Ecology 6: 831-842. http://dx.doi.org/10.1111/j.1365-294X.1997.tb00137.x

Golan-Goldhirsh, A., Barazani, O., Wang, Z.S., Khadka, D.K., Saunders, J.A., Kostiukovsky, V. & Rowland L. J. 2004. Genetic relationships among Mediterranean Pistacia species evaluated by RAPD and AFLP markers. Plant Systematics and Evolution 246: 9-18. http://dx.doi.org/10.1007/s00606-004-0132-4

Gómez Ortiz, A. & Savador i Franch, F. 1996. Acerca de la génesis y morfodinámica del glaciarismo de Sierra Nevada. In: Chacón J. & Rosua, J.L. (eds.), I Conferencia Internacional sobre Sierra Nevada, Granada. 1, pp. 233-260.

Günster, N. & Skowronek, A. 2001. Sediment-soil sequences in the Granada Basin as evidence for long- and short-term climatic changes during the Pliocene and Quaternary in the Western Mediterranean. Quaternary International 78: 17-32. http://dx.doi.org/10.1016/S1040-6182(00)00112-9

Gutiérrez Larena, B., Fuertes Aguilar, J. & Nieto Feliner, G. 2002. Glacial-induced altitudinal migrations in Armeria (Plumbaginaceae) inferred from patterns of chloroplast DNA haplotype sharing. Molecular Ecology 11: 1965-1974. http://dx.doi.org/10.1046/j.1365-294X.2002.01594.x PMid:12296941

Gutiérrez Larena, B., Fuertes Aguilar, J. & Nieto Feliner, G. 2004. Morphometric and molecular evidence for taxonomic recognition of a new subspecies of Armeria filicaulis (Plumbaginaceae). Anales del Jardín Botánico de Madrid 61: 35-48

Gutiérrez Larena, B., Fuertes Aguilar, J. & Nieto Feliner, G. 2006. Dispersal across Southern Iberian refugia? Integrating RAPDs, sequence data and morphometrics in Armeria (Plumbaginaceae). Folia Geobotanica 41: 305-322. http://dx.doi.org/10.1007/BF02904944

Harlan, J.R. & De Wet J.M.J. 1963. The compilospecies concept. Evolution 17: 497–501. http://dx.doi.org/10.2307/2407101

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.

Hewitt, G.M. 1999. Post-glacial recolonization of European biota. Biological Journal of the Linnean Society 68: 87-112. http://dx.doi.org/10.1111/j.1095-8312.1999.tb01160.x

Hewitt, G.M. 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907-913. http://dx.doi.org/10.1038/35016000 PMid:10879524

Holderegger, R., Stehlik, I. & Abbott, R.J. 2002. Molecular analysis of the Pleistocene history of Saxifraga oppositifolia in the Alps. Molecular Ecology 11: 1409-1418. http://dx.doi.org/10.1046/j.1365-294X.2002.01548.x PMid:12144661

Hubisz, M.J., Falush, D., Stephens, M. & Pritchard. J.K.2009. Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9: 1322-1332. http://dx.doi.org/10.1111/j.1755-0998.2009.02591.x PMid:21564903

Jones, C.J., Edwards, K.J., Castaglione, S., Winfield, M.O., Sala, F., van de Wiel, C., Bredemeijer, G., Vosman, B., Matthes, M., Daly, A., Brettschneider, R., Bettini, P., Buiatti, M., Maestri, E., Malcevschi, A., Marmiroli, N., Aert, R., Volckaert, G., Rueda, J., Linacero, R., Vazquez, A. & Karp, A. 1997. Reproducibility testing of RAPD, AFLP and SSR markers in plants by a network of European laboratories. Molecular Breeding 3: 381-390. http://dx.doi.org/10.1023/A:1009612517139

Jordano, P. & Godoy, J.A. 2000. RAPD variation and population genetic structure in Prunus mahaleb (Rosaceae), an animal-dispersed tree. Molecular Ecology 9: 1293-1305. http://dx.doi.org/10.1046/j.1365-294x.2000.01009.x PMid:10972769

Kropf, M., Comes, H.P. & Kadereit, J.W. 2006. Long-distance dispersal vs vicariance: The origin and genetic diversity of alpine plants in the Spanish Sierra Nevada. New Phytologist 172: 169-184. http://dx.doi.org/10.1111/j.1469-8137.2006.01795.x PMid:16945099

Kropf, M., Comes, H.P. & Kadereit, J.W. 2008. Causes of the genetic architecture of south-west European high mountain disjuncts. Plant Ecology & Diversity 1: 217-228

Legendre, P. & Legendre, L. 1998. Numerical Ecology. 2nd English Edition. Development in Environmental Modelling 20. Elsevier.

Lobo, J.M., Castro, I. & Moreno, J.C. 2001. Spatial and environmental determinants of vascular plant species richness distribution in the Iberian Peninsula and Balearic Islands. Biological Journal of the Linnean Society 73: 233-253. http://dx.doi.org/10.1111/j.1095-8312.2001.tb01360.x

López González, G. 1990. Arenaria. In: Castroviejo, S., Laínz, M., López González G., Montserrat P., Muñoz Garmendia F., Paiva, J. & Villar, L. (eds.), Flora iberica 2: 172-224. CSIC, Madrid.

Lorenz, M., Weihe, A. & Börner, T. 1994. DNA fragments of organellar origin in random amplified polymorphic DNA (RAPD) patterns of sugar beet (Beta vulgaris L.). Theoretical and Applied Genetics 88: 775-779. http://dx.doi.org/10.1007/BF01253985

Lorite, J. & Valle, F. 1999. Bases para la elaboración de modelos de gestión de la vegetación en la Sierra Nevada almeriense. Conclusiones del Encuentro Medioambiental Almeriense. Universidad de Almería. 114 pp.

Martin, L.J. & Cruzan, M.B. 1999. Patterns of hybridization in the Piriqueta caroliniana complex in central Florida: evidence for an expanding hybrid zone. Evolution 53: 1037-1049. http://dx.doi.org/10.2307/2640809

Médail, F. & Quézel, P. 1997. Hot-spots analysis for conservation of plant diversity in the Mediterranean Basin. Annals of the Missouri Botanical Garden 84: 112-127. http://dx.doi.org/10.2307/2399957

Miller, M. 1997. Tools for population genetic analysis (TFPGA) 1.3: A windows program for the analysis of allozyme and molecular population genetic data.

Molero Mesa, J. 1994. Baetic and Sub-Baetic Mountains, Spain. In: Davis S.D., Heywood V.H. & Hamilton A.C. (eds.), Centres of Plant Diversity. A Guide and Strategy for their Conservation 1: Europe, Africa, SW Asia and the Middle East: pp 55-58. IUCN Publication Unit, Cambridge.

Morgan-Richards, M. & Wolff, K. 1999. Genetic structure and differentiation of Plantago major reveals a pair of sympatric sister species. Molecular Ecology 8:1027-1036. http://dx.doi.org/10.1046/j.1365-294x.1999.00665.x

Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of USA 70: 3321-3323. http://dx.doi.org/10.1073/pnas.70.12.3321

Nieto Feliner, G. 1993. Erysimum. In: Castroviejo, S., Laínz, M., López González, G., Montserrat, P., Muñoz Garmendia, F., Paiva, J. & Villar, L. (eds.), Flora iberica 4: 48-76. CSIC, Madrid.

Nieto Feliner, G. 2011. Southern European glacial refugia: A tale of tales. Taxon 60: 365-372.

Nieto Feliner, G., Fuertes Aguilar, J & Rosselló, J.A. 2001, A new species of Armeria (Plumbaginaceae) from southern Spain with molecular and morphometric evidence on its origin. Botanical Journal of the Linnean Society 135: 71-84.

Nieto Feliner, G., Fuertes Aguilar J. & Rosselló, J.A. 2002. Reticulation or divergence: the origin of a rare serpentine endemic assessed with chloroplast, nuclear and RAPD markers. Plant Systematics and Evolution 231: 19-38. http://dx.doi.org/10.1007/s006060200009

Nieto Feliner, G., Gutiérrez Larena, B. & Fuertes Aguilar, J. 2004. Fine-scale geographical structure, intra-individual polymorphism and recombination in nuclear ribosomal internal transcribed spacers in Armeria (Plumbaginaceae). Annals of Botany 93: 189-200. http://dx.doi.org/10.1093/aob/mch027 PMid:14707002

Nieto Feliner, G., Izuzquiza, A. & Lansac, A.R. 1996. Natural and experimental hybridization in Armeria (Plumbaginaceae): A. villosa subsp. carratracensis. Plant Systematics and Evolution 201: 163-177. http://dx.doi.org/10.1007/BF00989059

Nieto Feliner, G., Rosselló, J.A. & Fuertes Aguilar, J. 1998. A new subspecies of Armeria filicaulis (Plumbaginaceae) from Sierra Nevada (Southern Spain). Anales del Jardín Botánico de Madrid 56: 162-164.

Nybom, H. 2004. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology 13: 1143-1155. http://dx.doi.org/10.1111/j.1365-294X.2004.02141.x PMid:15078452

Nybom, H. & Bartish, I.V. 2000. Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspectives in Plant Ecology, Evolution and Systematics 3/2: 93-114. http://dx.doi.org/10.1078/1433-8319-00006

Palacios, C. & González Candelas, F. 1997. Analysis of population genetic structure and variability using RAPD markers in the endemic and endangered Limonium dufourii (Plumbaginaceae). Molecular Ecology 6: 1107-1121. http://dx.doi.org/10.1046/j.1365-294X.1997.00283.x PMid:9421917

Peever, T.L. & Milgroom, M.G.1994. Genetic structure of Pyreno phora teres populations determined with random amplified polymorphic DNA markers. Canadian Journal of Botany 72: 915-923. http://dx.doi.org/10.1139/b94-116

Petit, R.J., Aguinagalde, I., de Beaulieu J. L., Bittkau, C., Brewer, S., Cheddadi, R., Ennos, R., Fineschi, S., Grivet, D., Lascoux, M., Mohanty, A., Mu.ller-Starck, G., Demesure-Musch, B., Palmé, A., Martín, J.P., Rendell, S. & Vendramin, G.G. 2003. Glacial Refugia: Hotspots but Not Melting Pots of Genetic Diversity. Science 300: 1563-1565.

Petit, R.J., Csaikl, U.M., Bordács, S., Burg, K., Coart, E., Cottrell, J., van Dam, B.C., Deans, J.D., Dumolin-Lapègue, S., Fineschi, S., Finkelday, R., Gillies, A., Glaz, I., Goicoechea, P.G., Jensen, J.S., König, A., Lowe, A.J., Madsen, S.F., Mátyás, G., Munro, R.C., Pemonge, M.-H., Popescu, F., Slade, D, Tabbener, H., Taurchini, D., de Vries, S.M.G., Ziegenhagen, B. & Kremer, A. 2002. Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecology and Management 156: 5-26. http://dx.doi.org/10.1016/S0378-1127(01)00645-4

Piñeiro, R., Widmer, A., Fuertes Aguilar, J. & Nieto Feliner, G. 2011. Introgression in peripheral populations and colonization shape the genetic structure of the coastal shrub Armeria pungens. Heredity 106: 228-240. http://dx.doi.org/10.1038/hdy.2010.46 PMid:20424642

Pons, A. & Reille, M. 1988. The Holocene and Upper Pleistocene pollen record from Padul (Granada, Spain), A new study. Palaeogeography, Palaeoclimatology, Palaeoecology. 66: 243-263. http://dx.doi.org/10.1016/0031-0182(88)90202-7

Pritchard, J.K, Stephens, M. & Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959. PMid:10835412    PMCid:1461096

Raffl, C., Schönswetter, P. & Erschbamer, B. 2006. 'Sax-sess' – genetics of primary succession in a pioneer species on two parallel glacier forelands. Molecular Ecology 15: 2433-2440. http://dx.doi.org/10.1111/j.1365-294X.2006.02964.x PMid:16842417

Rieseberg, L.H. 1996. Homology among RAPD fragments in interspecific comparisons. Molecular Ecology 5: 99-105. http://dx.doi.org/10.1111/j.1365-294X.1996.tb00295.x

Rivas-Martínez, S., Fernández González, F. & Sánchez Mata, D. 1986. Datos sobre la Vegetación del Sistema Central y Sierra Nevada. Opuscula Botanica Pharmaciae Complutensis 2: 3-136.

Rohlf, F.J. 2002. NTSYS-pc, numerical taxonomy and multivariate analysis system. Version 2.11a, User guide. New York: Exeter software.

Ronikier, M., Costa, A., Aguilar, J.F., Feliner, G.N., Küpfer, P. & Mirek, Z. 2008. Phylogeography of Pulsatilla vernalis (L.) Mill. (Ranunculaceae): Chloroplast DNA reveals two evolutionary lineages across central Europe and Scandinavia. Journal of Biogeography 35: 1650-1664. http://dx.doi.org/10.1111/j.1365-2699.2008.01907.x

Saitou, N. & Nei, M. 1987. The neighbour-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425. PMid:3447015

Salazar, C. 2009. Armeria Willd. In: Blanca, G., Cabezudo, B., Cueto, M., Fernández López, C. & Morales Torres, C. (eds.), Flora Vascular de Andalucía Oriental 2: 210-217. Consejería de Medio Ambiente, Sevilla.

Sale, M.M., Potts, B.M., West, A.K. & Reid, J.B. 1996. Molecular differentiation within and between Eucalyptus ridsonii, E. amygdalina and their hybrids using RAPD markers. Australian Journal of Botany 44: 559-569. http://dx.doi.org/10.1071/BT9960559

Salinas, M.J. 2009. Erodium L’Hér. In: Blanca, G., Cabezudo, B., Cueto, M., Fernández López, C. & Morales Torres, C. (eds.), Flora Vascular de Andalucía Oriental 3: 228-237. Consejería de Medio Ambiente, Sevilla.

Schneider, S., Roessli, D. & Excoffier, L. 2000. ARLEQUIN, Version 2.001: a Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory. University of Geneva.

Schönswetter, P, Stehlik, I, Holderegger, R. & Tribsch, A 2005. Molecular evidence for glacial refugia of mountain plants in the European Alps. Molecular Ecology 14: 3547-3555. http://dx.doi.org/10.1111/j.1365-294X.2005.02683.x PMid:16156822

Schulte, L. 2002. Climatic and human influence on river systems and glacier fluctuations in southeast Spain since the Last Glacial Maximum. Quaternary International 93-94: 85-100. http://dx.doi.org/10.1016/S1040-6182(02)00008-3

Segarra-Moragues, J. G. & Catalán, P. 2003. Life history variation between species of the relictual genus Borderea (Dioscoreaceae): phylogeography, genetic diversity, and population genetic structure assessed by RAPD markers. Biological Journal of the Linnean Society 80: 483-498. http://dx.doi.org/10.1046/j.1095-8312.2003.00247.x

Simón, M., Sánchez, S. & García, I. 2000. Soil-landscape evolution on a Mediterranean high mountain. Catena 39: 211-231. http://dx.doi.org/10.1016/S0341-8162(99)00088-0

Skroch, P. & Nienhuis, J. 1995. Impact of scoring error and reproducibility of RAPD data on RAPD based estimates of genetic distance. Theoretical and Applied Genetics 91: 1086-1091. http://dx.doi.org/10.1007/BF00223923

Steen, S.W., Gielly, L., Taberlet, P. & Brochmann, C. 2000. Same parental species, but different taxa: molecular evidence for hybrid origins of the rare endemics Saxifraga opdalensis and S. svalbardensis (Saxifragaceae). Botanical Journal of the Linnean Society 132: 153-164.

Stehlik, I. 2000. Nunataks and peripheral refugia for alpine plants during quaternary glaciation in the middle part of the Alps. Botanica Helvetica 110: 25-30.

Stehlik, I. 2003. Resistance or emigration? Response of alpine plants to the ice ages. Taxon 52: 499-510. http://dx.doi.org/10.2307/3647448

Stehlik, I., Schneller, J.J. & Bachmann, K. 2002. Immigration and in situ glacial survival of the low-alpine Erinus alpinus (Scrophulariaceae). Biological Journal of the Linnean Society 77: 87-103. http://dx.doi.org/10.1046/j.1095-8312.2002.00094.x

Steward, Jr., C.N. & Excoffier, L. 1996. Assessing population genetic structure and variability with RAPD data: Application to Vaccinium macrocarpon (American cranberry). Journal of Evolutionary Biology 9: 153-171. http://dx.doi.org/10.1046/j.1420-9101.1996.9020153.x

Swensen, S.M., Allan, G.J., Howe, M., Elisens, W.J., Junak, S.A. & Rieseberg, L.H. 1995. Genetic analysis of the endangered island endemic Malacothamnus fasciculatus (Nutt.) Greene var. nesioticus (Rob.) Kearn., (Malvaceae). Conservation Biology 9: 404-415. http://dx.doi.org/10.1046/j.1523-1739.1995.9020404.x

Swofford, D.L. 2002. PAUP*: Phylogenetic Analysis Using Parsimony and other methods, Version 4.0. Beta 10. Sinauer, Sunderland, MA.

Tribsch, A. & Schönswetter, P. 2003. Patterns of endemism and comparative phylogeography confirm palaeo-environmental evidence for Pleistocene refugia in the Eastern Alps. Taxon 52: 477-497. http://dx.doi.org/10.2307/3647447

Weising, K., Nybom, H., Wolf, K. & Meyer, W. 1995. DNA fingerprinting in plant and fungi. CRC Press. Boca Raton, FL.

Williams, J., Kubelik, A., Livak, K., Rafalski, J. & Tingey, S. 1990. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Research 18: 6531-6535. http://dx.doi.org/10.1093/nar/18.22.6531 PMid:1979162    PMCid:332606

Winkler, M., Tribsch, A., Paun, O., Englisch, T. & Schönswetter, P. 2010. Pleistocene distribution range shifts were accompanied by breeding system divergence within Hornungia alpina (Brassicaceae) in the Alps. Molecular Phylogenetics and Evolution 54: 571-582 http://dx.doi.org/10.1016/j.ympev.2009.08.009 PMid:19695334

Wolfe, A.D. & Liston, A. 1998. Contributions of PCR-based methods to plant systematics and evolutionary biology. In: Soltis, D.E., Soltis, P.S. & Doyle, J.J. (eds.), Molecular Systematics of Plants II: DNA Sequencing: 43-86. Kluwer, New York.

Yüzbasjoglu, E., DadandI, M.Y. & Özcan, S. 2008. Natural hybridization between Phlomis lycia D. Don × P. bourgaei Boiss. (Lamiaceae) revealed by RAPD markers. Genetica 133: 13-20. http://dx.doi.org/10.1007/s10709-007-9177-y PMid:17705021




Copyright (c) 2011 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us: anales@rjb.csic.es

Technical support: soporte.tecnico.revistas@csic.es