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Complex population genetic structure in the endemic Canary Island pine revealed using chloroplast microsatellite markers

Abstract

The Canary archipelago, located on the northwestern Atlantic coast of Africa, is comprised of seven islands aligned from east to west, plus seven minor islets. All the islands were formed by volcanic eruptions and their geological history is well documented providing a historical framework to study colonization events. The Canary Island pine (Pinus canariensis C. Sm.), nowadays restricted to the westernmost Canary Islands (Gran Canaria, Tenerife, La Gomera, La Palma and El Hierro), is considered an old (Lower Cretaceous) relic from an ancient Mediterranean evolutionary centre. Twenty seven chloroplast haplotypes were found in Canary Island pine but only one of them was common to all populations. The distribution of haplotypic variation in P. canariensis suggested the colonization of western Canary Islands from a single continental source located close to the Mediterranean Basin. Present-day populations of Canary Island pine retain levels of genetic diversity equivalent to those found in Mediterranean continental pine species, Pinus pinaster and Pinus halepensis. A hierarchical analysis of variance (AMOVA) showed high differentiation among populations within islands (approximately 19%) but no differentiation among islands. Simple differentiation models such as isolation by distance or stepping-stone colonization from older to younger islands were rejected based on product-moment correlations between pairwise genetic distances and both geographic distances and population-age divergences. However, the distribution of cpSSR diversity within the islands of Tenerife and Gran Canaria pointed towards the importance of the role played by regional Pliocene and Quaternary volcanic activity and long-distance gene flow in shaping the population genetic structure of the Canary Island pine. Therefore, conservation strategies at the population level are strongly recommended for this species.

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References

  1. Aboal JR, Jiménez MS, Morales D, Gil P (2000) Effect of thinning on throughfall in Canary Islands pine forest – the role of fog. J Hydrol 238:218–230

    Article  Google Scholar 

  2. Ancochea E, Fúster JM, Ibarrola E, Cendrero A, Coello J, Hernán F, Cantagrel JM, Jamond C (1990) Volcanic evolution of the island of Tenerife (Canary Islands) in the light of new K-Ar data. J Volcanol Geotherm Res 44:231–249

    CAS  Google Scholar 

  3. Austerlitz F, Mariette S, Machon N, Gouyon PH, Godelle B (2000) Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154:1309–1321

    CAS  PubMed  Google Scholar 

  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA

  5. Baldwin BG, Crawford DJ, Francisco-Ortega J, Kin S-C, Sang T, Stuessy TF (1988) Molecular phylogenetic insights on the origin and evolution of oceanic island plants. In: Soltis DE, Soltis P, Doyle JJ (eds) Molecular systematics of plants. II. DNA sequencing. Kluwer Academic Publishers, New York, USA, pp 410–441

  6. Böhle UR, Hilger HH, Martin WF (1996) Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proc Natl Acad Sci USA 93:11,740–11,745

    Article  Google Scholar 

  7. Bramwell D (1976) The endemic flora of the Canary Islands: distribution, relationships and phytogeography. In: Kunkel G (ed) Biogeography and ecology in the Canary Islands. W. Junk, The Hague, pp 207–240

  8. Bramwell D (1990) Conserving biodiversity in the Canary Islands. Ann Missouri Bot Gard 77:28–37

    Google Scholar 

  9. Brown RP, Pestano J (1998) Phylogeography of skinks (Chalcides) in the Canary Islands inferred from mitochondrial DNA sequences. Mol Ecol 7:1183–1191

    Article  CAS  PubMed  Google Scholar 

  10. Climent J, Gil L, Tuero M (1996) Regiones de procedencia de Pinus canariensis Chr. Sm. Ex DC. DGCONA-MAPA, Madrid

  11. Coello J, Cantagrel JM, Hernán F, Fuster JM, Ibarrola E, Ancoechea E, Casquet C, Jamond C, Díaz de Terán JR, Cendrero A (1992) Evolution of the eastern volcanic ridge of the Canary Islands based on new K-Ar data. J Volcanol Geotherm Res 53:251–274

    CAS  Google Scholar 

  12. Crandall KA, Templeton AR (1996) Applications of intraspecific phylogenetics. In: Harvey PH, Brown AJL, Smith JM (eds) New uses for new phylogenies. Oxford University Press, Oxford

  13. De la Rúa P, Galián J, Serrano J, Moritz RFA (2001) Genetic structure and distinctness of Apis mellifera L. populations from Canary Islands. Mol Ecol 10:1733–1742

    Article  PubMed  Google Scholar 

  14. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  15. Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966

    Article  CAS  PubMed  Google Scholar 

  16. Emerson BC, Oromí P, Hewitt GM (1999) MtDNA phylogeography and recent intra-island diversification among Canary Island Calathus beetles. Mol Phylog Evol 13:149–158

    Article  CAS  Google Scholar 

  17. Emerson BC, Oromí P, Hewitt GM (2000) Interpreting colonization of the Calathus (Coleoptera: Carabidae) on the Canary Islands and Madeira through the application of the parametric bootstrap. Evolution 54:2081–2090

    CAS  PubMed  Google Scholar 

  18. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  19. Francisco-Ortega J, Jansen RK, Santos-Guerra A (1996) Chloroplast DNA evidence of colonization, adaptive radiation, and hybridization in the evolution of the Macaronesian flora. Proc Natl Acad Sci USA 93:4085–4090

    Article  CAS  PubMed  Google Scholar 

  20. Funck T, Dickmann T, Rihm R, Krastel S, Lykke-Andersen H, Schmincke H-U (1996) Reflecting seismic investigations in the volcaniclastic apron of Gran Canaria and implications for its volcanic evolution. Geophysical J Int 125:519–536

    Google Scholar 

  21. Gil L, Climent J, Nanos N, Mutke S, Ortiz I, Schiller G (2002) Cone morphology variation in Pinus canariensis Sm. Plant Syst Evol 235:35–51

    Article  Google Scholar 

  22. Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471

    CAS  PubMed  Google Scholar 

  23. Grant PR (1986) Ecology and evolution of Darwin's Finches. Princeton University Press, Princeton, New Jersy

  24. Gregor HJ (1980) Funde von Pinus canariensis Ch. Smith fossilis aus dem Neogen von La Palma Kanarische Inselm. Vieraea 9:57–64

    Google Scholar 

  25. Hamrick JL, Godt MJ, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New For 6:95–124

    Google Scholar 

  26. Hess J, Kadereit JW, Vargas P (2000) The colonization history of Olea europaea L. in Macaronesia based on internal transcribed spacer 1 (ITS-1) sequences, randomly amplified polymorphic DNAs (RAPD), and intersimple sequence repeats (ISSR). Mol Ecol 9:857–868

    Article  CAS  PubMed  Google Scholar 

  27. Hewitt GM (2001) Speciation, hybrid zones and phylogeography – or seeing genes in space and time. Mol Ecol 10:537–549

    Article  CAS  PubMed  Google Scholar 

  28. Juan C, Oromí P, Hewitt GM (1995) Mitochondrial DNA phylogeny and sequential colonization of Canary islands by darkling beetles of the genus Pimelia (Tenebrionidae). Proc R Soc B 261:173–180

    CAS  Google Scholar 

  29. Juan C, Oromí P, Hewitt GM (1996) Phylogeny of the genus Hegeter (Tenebrionidae, Coleoptera) and its colonization of the Canary Islands deduced from Cytochrome Oxidase I mitochondrial DNA sequences. Heredity 76:392–403

    CAS  PubMed  Google Scholar 

  30. Juan C, Emerson BC, Oromí P, Hewitt GM (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. TREE 15:104–109

    Article  PubMed  Google Scholar 

  31. Kim S-C, Crawford DJ, Francisco-Ortega J, Santos-Guerra A (1996) A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation. Proc Natl Acad Sci USA 93:7743–7748

    Article  CAS  PubMed  Google Scholar 

  32. Klaus W (1989) Mediterranean pines and their history. Plant Syst Evol 162:133–163

    Google Scholar 

  33. Korol L, Gil L, Climent J, Zehavi A, Schiller G (1999) Canary Islands pine (Pinus canariensis Chr. Sm. ex DC) 2. Gene flow among native populations. For Genet 6:277–282

    Google Scholar 

  34. Ledig FT (1998) Genetic variation in Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 251–280

  35. Liston A, Robinson WA, Piñero D, Álvarez-Buylla ER (1999) Phylogenetics of Pinus (Pinaceae) based on nuclear ribosomal DNA Internal Transcribed Spacer region sequences. Mol Phylog Evol 11:95–109

    CAS  Google Scholar 

  36. López G, Kamiya K, Harada K (2002) Phylogenetic relationships of Diploxilon pines (subgenus Pinus) based on plastid sequence data. Int J Plant Sci 163:737–747

    Article  Google Scholar 

  37. Loveless MD (1992) Isozyme variation in tropical trees: patterns of genetic organization. New For 6:67–94

    Google Scholar 

  38. Machado-Yanes MC (1996) Reconstrucción paleoecológica y etnoarqueológica por medio del análisis antracológico. La cueva de Villaverde (Fuerteventura). In: Ramil-Rego P, Fernández-Rodríguez C, Rodríguez-Guitián M (eds) Biogeografía Pleistocena-Holocena de la Península Ibérica. Universidad de Santiago, Spain, pp 261–274

  39. Mantel NA (1967) The detection of disease clustering and a generalizated regression approach. Cancer Res 27:91–99

    Google Scholar 

  40. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  41. Nogales M, López M, Jiménez-Asensio J, Larruga JM, Hernández M, González P (1998) Evolution and biogeography of the genus Tarentola (Sauria: Gekkonidae) in the Canary Islands, inferred from mitochondrial DNA sequences. J Evol Biol 11:481–494

    Article  Google Scholar 

  42. Pinto FM, Brehm A, Hernández M, Larruga JM, González AM, Cabrera VM (1997) Population genetic structure and colonization sequence of Drosophila subobscura in the Canaries and Madeira Atlantic islands as inferred by autosomal, sex-linked and mtDNA traits. J Hered 88:108–114

    CAS  PubMed  Google Scholar 

  43. Rees DJ, Emerson BC, OromíP, Hewitt GM (2001) Mitochondrial DNA, ecology and morphology: interpreting the phylogeography of the Nesotes (Coleoptera: Tenebrionidae) of Gran Canaria (Canary Islands). Mol Ecol 10:427–434

    Article  CAS  PubMed  Google Scholar 

  44. Sahuquillo E, Lumaret R (1999) Chloroplast DNA variation in Dactylis glomerata L. taxa endemic to the Macaronesian islands. Mol Ecol 8:1797–1803

    Article  CAS  PubMed  Google Scholar 

  45. Schiller G, Korol L, Ungar ED, Zehavi A, Gil L, Climent J (1999) Canary islands pine (Pinus canariensis Chr. Sm. ex DC) 1. Differentiation among native populations in their isoenzymes. For Genet 6:257–276

    Google Scholar 

  46. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2000: a software for population genetic data analysis. Genetic and Biometry Laboratory, University of Geneva, Switzerland

  47. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed  Google Scholar 

  48. Thorpe RS, McGregor DP, Cumming AM, Jordan WC (1994) DNA evolution and colonization sequence of island lizards in relation to geological history: mtDNA, RFLP, cytochrome B, cytochrome oxidase, 12S rRNA and nuclear RAPD analysis. Evolution 48:230–240

    CAS  Google Scholar 

  49. Vendramin GG, Lelli L, Rossi P, Morgante M (1996) A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5:595–598

    CAS  PubMed  Google Scholar 

  50. Wang XR, Tsumura Y, Yoshimaru H, Nagasaka K, Szmidt AE (1999) Phylogenetic relationships of Eurasian pines (Pinus, Pinaceae) based on chloroplast rbcL, matK, rpl 20-rps18 spacer, and trnV intron sequences. Am J Bot 86:1742–1753

    CAS  PubMed  Google Scholar 

  51. Zheng Y-Q, Ennos RA (1999) Genetic variability and structure of natural and domesticated populations of Caribbean pine (Pinus caribaea Morelet). Theor Appl Genet 98:765–771

    Article  Google Scholar 

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Acknowledgements

Brent Emerson and Ricardo Alía's valuable contributions to discussions on the original manuscript are much appreciated. We are grateful to Esther Pérez for field work and to Leonie Woodin who revised the English language. This work was supported by the Insular Administration (Cabildo) of Tenerife and by the Viceconsejería de Medio Ambiente (Canary Islands Government). Technical support was also provided by the Cabildo of Gran Canaria. All the experiments conducted during this study comply with the current laws of Spain.

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Correspondence to L. Gil.

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Communicated by D.B. Neale

A. Gómez and S.C. González-Martínez as joint authors

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Gómez, A., González-Martínez, S.C., Collada, C. et al. Complex population genetic structure in the endemic Canary Island pine revealed using chloroplast microsatellite markers. Theor Appl Genet 107, 1123–1131 (2003). https://doi.org/10.1007/s00122-003-1320-2

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Keywords.

  • Colonization
  • Gene diversity
  • Genetic structure
  • Pinus canariensis
  • Oceanic islands