Biogeographic history of the threatened species Araucaria araucana (Molina) K. Koch and implications for conservation: A case study with organelle DNA markers

Conservation Genetics

Volumn 11, Issue 3, 2010, Pages 951-963

  Marchelli, P ^a,b   Baier, C ^c,d   Mengel, C ^c   Ziegenhagen, B ^c   Gallo, L A ^a  

^a Inst Nac de Tecnol Agropecuaria   (Argentina)

^b Consejo Nacional de Investigaciones Científicas y Técnicas ^*  (Argentina)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Chloroplast DNA; Fragmentation; Geographical genetic structure; Mitochondrial DNA; Monkey puzzle tree; Patagonian temperate forests

Indexed keywords

CHLOROPLAST; CONIFEROUS TREE; CONSERVATION GENETICS; ENDANGERED SPECIES; GENETIC DIFFERENTIATION; GENETIC MARKER; GENETIC STRUCTURE; GLACIATION; HABITAT FRAGMENTATION; HISTORICAL GEOGRAPHY; HYPOTHESIS TESTING; MITOCHONDRIAL DNA; NATIONAL PARK; PLEISTOCENE; SPECIES CONSERVATION; STEPPE; TEMPERATE FOREST;

SOUTH AMERICA;

ARAUCARIA ARAUCANA; PINACEAE;

EID: 77952880299     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-009-9938-5     Document Type: Article

References (90)

1. Amos W, Sawcer SJ, Feakes RW, Rubinsztein DC (1996) Microsatellites show mutational bias and heterozygote instability. Nat Genet 13: 390-391. doi: 10. 1038/ng0896-390.
2. Azpilicueta MM, Marchelli P, Gallo LA (2009) The effects of Quaternary glaciations in Patagonia as evidenced by chloroplast DNA phylogeography of Southern beech Nothofagus oblique. Tree Genet Genomes (in press).
3. Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196: 80-83. doi: 10. 1016/0003-2697(91)90120-I.
4. Bekessy S, Allnutt T, Premoli A et al (2002) Genetic variation in the monkey puzzle tree (Araucaria araucana (Molina) K. Koch), detected using RAPDs. Heredity 88: 243-249. doi: 10. 1038/sj. hdy. 6800033.
5. Bekessy SA, Ennos RA, Burgman MA, Newton AC, Ades PK (2003) Neutral DNA markers fail to detect genetic divergence in an ecologically important trait. Biol Conserv 110: 267-275. doi: 10. 1016/S0006-3207(02)00225-2.
6. Bennett K, Haberle S, Lumley S (2000) The last glacial-holocene transition in souther Chile. Science 290: 325-328. doi: 10. 1126/science. 290. 5490. 325.
7. Bucci G, González-Martínez S, Le Prevost G et al (2007) Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed y chloroplast microsatellite markers. Mol Ecol 16: 2137-2153. doi: 10. 1111/j. 1365-294X. 2007. 03275. x.
8. Burns BR (1993) Fire-induced dynamics of Araucaria araucana-Nothofagus antartica forest in the southern Andes. J Biogeogr 20: 669-685. doi: 10. 2307/2845522.
9. De Castillo A, Gavidia I, Perez-Bermudez P, Segura J (1995) PEG precipitation, a required step for PCR amplification of DNA from wild plants of Digitalis obscura L. Biotechniques 18: 766-768.
10. Demesure B, Sodzi N, Petit R (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4: 129-131. doi: 10. 1111/j. 1365-294X. 1995. tb00201. x.
11. Demesure B, Comps B, Petit R (1996) Chloroplast DNA Phylogeography of the Common Beech (Fagus sylvatica L.) in Europe. Evol Int J Org Evol 50: 2515-2520. doi: 10. 2307/2410719.
12. Duminil J, Pemonge MH, Petit R (2002) A set of 35 consensus primer pairs amplifying genes and introns of plant mitochondrial DNA. Mol Ecol Notes 2: 428-430. doi: 10. 1046/j. 1471-8286. 2002. 00263. x.
13. Dumolin S, Demesure B, Petit R (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91: 1256. doi: 10. 1007/BF00220937.
14. Dumolin-Lapègue S, Pemonge MH, Petit R (1997) An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 6: 393-397. doi: 10. 1046/j. 1365-294X. 1997. 00193. x.
15. Dupanloup J, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11: 2571-2581. doi: 10. 1046/j. 1365-294X. 2002. 01650. x.
16. Echt CS, DeVerno L, Anzidei M, Vendramin GG (1998) Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Mol Ecol 7: 307-316. doi: 10. 1046/j. 1365-294X. 1998. 00350. x.
17. Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17: 1170-1188. doi: 10. 1111/j. 1365-294X. 2007. 03659. x.
18. El Mousadik A, Petit R (1996) Chloroplast DNA phylogeography of the argan tree of Morocco. Mol Ecol 5: 547-555. doi: 10. 1046/j. 1365-294X. 1996. 00123. x.
19. Eriksson O, Ehrlen J (2001) Landscape fragmentation and the viability of plant populations. In: Silvertown J, Antonovics J (eds) Integrating ecology and evolution in a spatial context. Blackwell Science, Oxford, pp 157-175.
20. 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.
21. Farjon A, Page C (1999) Conifers: status survey and conservation action plan. IUCN/SSC Conifer Specialist Group, Cambridge.
22. Flint R, Fidalgo F (1964) Glacial geology of the east flank of the Argentine Andes between latitude 39°10′S and latitude 41°20′S. Geol Soc Am Bull 75: 335-352. doi: 10. 1130/0016-7606(1964)75[335: GGOTEF]2. 0. CO; 2.
23. Flint R, Fidalgo F (1969) Glacial drift in the eastern Argentine Andes between latitude 41°10′S and latitude 43°10′S. Geol Soc Am Bull 80: 1043-1052. doi: 10. 1130/0016-7606(1969)80[1043: GDITEA]2. 0. CO; 2.
24. Gallo L, Izquierdo F, Sanguinetti LJ (2004) Araucaria araucana forest genetic resources in Argentina. In: Vinceti B, Amaral W, Meilleur B (eds) Challenges in managing forest genetic resources for livelihoods: examples from Argentina and Brazil. IPGRI, Rome, pp 105-131.
25. Gomez A, Vendramin G, Gonzales-Martínez S, 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. Divers Distrib 11: 257-263. doi: 10. 1111/j. 1366-9516. 2005. 00152. x.
26. Gregorius HR (1991) Gene conservation and the preservation of adaptability. In: Seitz A, Loeschcke V (eds) Species conservation: a population-biological approach. Birkhäuser Verlag, Basel, pp 31-47.
27. Grivet D, Heinze B, Vendramin G, Petit R (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 1: 345-349. doi: 10. 1046/j. 1471-8278. 2001. 00107. x.
28. Gugerli F, Sperisen C, Büchler U et al (2001) The evolutionary split of Pinaceae from other conifers: evidence from an intron loss and a multigene phylogeny. Mol Phylogenet Evol 21: 167-175. doi: 10. 1006/mpev. 2001. 1004.
29. Hampe A, Petit R (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8: 461-467. doi: 10. 1111/j. 1461-0248. 2005. 00739. x.
30. Hanski I, Simberloff D (1997) The Metapopulation approach, its history, conceptual domain and application to conservation. In: Hanski I, Gilpin ME (eds) Metapopulation biology. Academic Press, Inc, New York, pp 5-26.
31. Hartl D, Clark A (1988) Principles of population genetics, 2nd edn. Sinauer Associates, Inc. Publishers, USA.
32. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59: 1633-1638.
33. Heinze B (2007) A database of PCR primers for the chloroplast genomes of higher plants. Plant Methods 3: 1-7. doi: 10. 1186/1746-4811-3-4.
34. Heuertz M, Hausman J-F et al (2004) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern european populations of the common ash (Fraxinus excelsior L). Evol Int J Org Evol 58: 976-988.
35. Heusser C, Lowell T, Heusser L, Hauser A, Björn G (1996) Full-glacial-late-glacial paleoclimate of the Southern Andes: evidence from pollen, beetle and glacial records. J Quat Sci 11: 173-184. doi: 10. 1002/(SICI)1099-1417(199605/06)11: 3< 173:: AID-JQS237> 3. 0. CO; 2-5.
36. Heusser CJ, LE Heusser, Lowell TV (1999) Paleoecology of the Southern Chilean Lake District-Isla Grande de Chiloe' during middle-late llanquihue glaciation and deglaciation. Geogr Ann 81 A: 231-284.
37. Hollin JT, Schilling DH (1981) Late Wiscosin-Weichselian Mountain Glaciers and Small Ice Caps. In: Denton GH, Hughes TJ (eds) The last great ice sheets. John Wiley & Sons, New York, pp 179-206.
38. Kaur D, Bhatnagar S (1984) Fertilization and formation of neocytoplasm in Agathis robusta. Phytomorphology 34: 56-60.
39. Kershaw AP, McGlone MS (1995) The Quaternary history of the southern conifers. In: Enright NJ, Hill RS (eds) Ecology of the southern conifers. Melbourne University Press, Melbourne, pp 30-63.
40. Koonjul P, Brandt W, Farrant J, Lindsey G (1999) Inclusion of polyvinylpyrrolidone in the polymerase chain reaction reverses the inhibitory effects of polyphenolic contamination of RNA. Nucleic Acids Res 27: 915-916. doi: 10. 1093/nar/27. 3. 915.
41. Lara A, Rutherford P, Montory C et al (1999) Mapeo de la Eco-región de los bosques Valdivianos. Bol Tecnico Fundacion Vida Silvestre Buenos Aires Argent 51: 1-27.
42. Liepelt S, Kuhlenkamp V, Anzidei M, Vendramin GG, Ziegenhagen B (2001) Pitfalls in determining size homoplasy of microsatellite loci. Mol Ecol Notes 1: 332-335. doi: 10. 1046/j. 1471-8278. 2001. 00085. x.
43. Liepelt S, Bialozyt R, Ziegenhagen B (2002) Wind-dispersed pollen mediates postglacial gene flow among refugia. Proc Natl Acad Sci USA 99: 14590-14594. doi: 10. 1073/pnas. 212285399.
44. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27: 209-220.
45. Marchelli P, Gallo L (2004) The combined role of glaciation and hybridization in shaping the distribution of genetic variation in a Patagonian southern beech. J Biogeogr 31: 451-460.
46. Marchelli P, Gallo L (2006) Multiple ice-age refugia in a southern beech of South America as evidenced by chloroplast DNA markers. Conserv Genet 7: 591-603. doi: 10. 1007/s10592-005-9069-6.
47. Marchelli P, Gallo L, Scholz F, Ziegenhagen B (1998) Chloroplast DNA markers revealed a geographical divide across Argentinean southern beech Nothofagus nervosa (Phil.) Dim. et Mil. distribution area. Theor Appl Genet 97: 642-646. doi: 10. 1007/s001220050940.
48. Markgraf V, Romero E, Villagran C (1996) History and paleoecology of South American Nothofagus forests. In: Veblen T, Hill R, Read J (eds) The ecology and biogeography of Nothofagus forests. Yale University Press, New Haven, pp 354-386.
49. Messier W, Li SH, Stewart CB (1996) The birth of microsatellites. Nature 381: 483. doi: 10. 1038/381483a0.
50. Montané J (1968) Paleo-indian remains from Laguna de Tagua Tagua, Central Chile. Science 161: 1137-1138. doi: 10. 1126/science. 161. 3846. 1137.
51. Moreno PI (1997) Vegetation and climate near Lago Llanquihue in the Chilean Lake District between 20, 200 and 9, 500 14 C yr BP. J Quat Sci 12: 485-500. doi: 10. 1002/(SICI)1099-1417(199711/12)12: 6< 485:: AID-JQS330> 3. 0. CO; 2-4.
52. Morgante M, Felice N, Vendramin GG (1998) Analysis of hypervariable chloroplast microsatellites in Pinus halepensis reveals a dramatic genetic bottleneck. In: Karp A, Isaac PG, Ingram DS (eds) Molecular tools for screening biodiversity. Chapman & Hall, London, pp 407-412.
53. Palmer J (1992) Mitochondrial DNA in plant systematics: applications and limitations. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Springer, Berlin, pp 36-49.
54. Palmer J, Stein D (1986) Conservation of chloroplast genome structure among vascular plants. Curr Genet 10: 823-833. doi: 10. 1007/BF00418529.
55. Parducci L, Szmidt AE (1999) PCR-RFLP analysis of cpDNA in the genus Abies. Theor Appl Genet 98: 802-808. doi: 10. 1007/s001220051137.
56. Pastorino M, Gallo L (2002) Quaternary evolutionary history of Austrocedrus chilensis a cypress native to the Andean-Patagonian Forest. J Biogeogr 29: 1167-1178. doi: 10. 1046/j. 1365-2699. 2002. 00731. x.
57. Pastorino MJ, Marchelli P, Milleron M, Soliani C, Gallo LA (2009) The effect of different glaciation patterns over the current genetic variation distribution of the southern beech Nothofagus antarctica (G. Forster) Oersted. Genetica 136: 79-88. doi: 10. 1007/s10709-008-9314-2.
58. Peakall R, Smouse P (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295. doi: 10. 1111/j. 1471-8286. 2005. 01155. x.
59. Peakall R, Ebert D, Scott LJ, Meagher PF, Offord CA (2003) Comparative genetic study confirms exceptionally low genetic variation in the ancient and endangered relictual conifer, Wollemia nobilis (Araucariaceae). Mol Ecol 12: 2331-2343. doi: 10. 1046/j. 1365-294X. 2003. 01926. x.
60. Petit R, Vendramin G (2006) Phylogeography of organelle DNA in plants: an introduction. In: Weiss S, Ferrand N (eds) Phylogeography of Southern European Refugia, evolutionary perspectives on the origins and conservation of European biodiversity. Springer Press, Amsterdam, pp 23-97.
61. Petit R, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12: 844-855. doi: 10. 1046/j. 1523-1739. 1998. 96489. x.
62. Petit R, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14: 689-701. doi: 10. 1111/j. 1365-294X. 2004. 02410. x.
63. Pons O, Petit R (1995) Estimation, variance and optimal sampling of gene diversity I. Haploid locus. Theor Appl Genet 90: 462-470. doi: 10. 1007/BF00221991.
64. Powell W, Morgante M, McDevitt R, Vendramin GG, Rafalsky JA (1995) Polymorphic simple sequence repeat regions in chloroplast genomes: applications to the population geneties of pines. Proc Natl Acad Sci USA 92: 7759-7763. doi: 10. 1073/pnas. 92. 17. 7759.
65. Premoli AC, Kitzberger T, Veblen TT (2000) Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides. J Biogeogr 27: 251-260. doi: 10. 1046/j. 1365-2699. 2000. 00402. x.
66. Pupko T, Graur D (1999) Evolution of microsatellites in the yeast Saccharomyces cerevisiae: role of length and number of repeated units. J Mol Evol 48: 313-316.
67. Rabassa J, Clapperton CM (1990) Quaternary glaciations of the Southern Andes. Quat Sci Rev 9: 153-174. doi: 10. 1016/0277-3791(90)90016-4.
68. Ribeiro M, Plomion C, Petit R, Vendramin G, Szmidt A (2001) Variation in chloroplast single-sequence repeats in Portuguese maritime pine (Pinus pinaster Ait). Theor Appl Genet 102: 97-103. doi: 10. 1007/s001220051623.
69. Robledo-Arnuncio JJ, Alia R, Gil L (2004) Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris. Mol Ecol 13: 2567-2577. doi: 10. 1111/j. 1365-294X. 2004. 02251. x.
70. Rose O, Falush D (1998) A threshold size for microsatellite expansion. Mol Biol Evol 15: 613-615.
71. Ruiz E, González F, Torres-Diaz C et al (2007) Genetic diversity and differentiation within and among Chilean populations of Araucaria araucana (Araucariaceae) based on allozyme variability. Taxon 56: 1221-1228.
72. Sanguinetti L, Maresca L, Gonzalez Peñalba M, Chauchard L, Lozano L (2002) Producción bruta de semillas de Araucaria araucana. Internal Report Lanin National Park.
73. Schlögl PS, Souza AP, Nodari RO (2007) PCR-RFLP analysis of non-coding regions of cpDNA in Araucaria angustifolia (Bert.) O. Kuntze. Genet Mol Biol 30: 423-427. doi: 10. 1590/S1415-47572007000300020.
74. Scott LJ, Sheperd MJ, Nikles DG, Henry RJ (2005) Low efficiency of pseudotestcross mapping design was consistent with limited genetic diversity and low heterozygosity in hoop pine (Araucaria cunninghamii, Araucariaceae). Tree Genet Genomes 1: 124-134. doi: 10. 1007/s11295-005-0022-0.
75. Soranzo N, Provan J, Powell W (1999) An example of mitochondrial length variation in the mitochondrial genome of conifers. Genome 42: 158-161. doi: 10. 1139/gen-42-1-158.
76. Sperisen C, Büchler U, Mátyás C (1998) Genetic Variation of Mitochondrial DNA Reveals Subdivision of Norway Spruce (Picea abies (L.) Karst.). In: Karp A, Isaac PG, Ingram DS (eds) Molecular tools for screening biodiversity. Chapman & Hall, London, pp 413-417.
77. Stefenon V, Nodari R, Guerra M (2004) Genética e conservação de Araucaria angustifolia: III. Protocolo de extração de DNA e capacidade informativa de marcadores RAPD para análise da diversidade genética em populações naturais. Biotemas 17: 47-63.
78. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17: 1105-1109. doi: 10. 1007/BF00037152.
79. Tang S, Dai W, Li M et al (2008) Genetic diversity of relictual and endangered plant Abies ziyuanensis (Pinaceae) revealed by AFLP and SSR markers. Genetica 133: 21-30. doi: 10. 1007/s10709-007-9178-x.
80. Templeton AR, Robertson RJ, Brisson J, Strasburg J (2001) Disrupting evolutionary processes: the effect of the habitat fragmentation on collared lizards in the Missouri Ozarks. Proc Natl Acad Sci USA 98: 5426-5432. doi: 10. 1073/pnas. 091093098.
81. Vendramin GG, Ziegenhagen B (1997) Characterization and inheritance of polymorphic plastid microsatellites in Abies. Genome 40: 857-864. doi: 10. 1139/g97-811.
82. Vendramin GG, Lelli L, Rossi P, Morgante M (1996) A set of primers for the amplification of 20 chloplast microsatellites in Pinaceae. Mol Ecol 5: 595-598. doi: 10. 1111/j. 1365-294X. 1996. tb00353. x.
83. Vendramin GG, Anzidei M, Madaghiele A, Bucci G (1998) Distribution of genetic diversity in Pinus pinaster Ait. as revealed by chloroplast microsatellites. Theor Appl Genet 97: 456-463. doi: 10. 1007/s001220050917.
84. Vendramin GG, Degen B, Petit R, Anzidei M, Madaghiele A, Ziegenhagen B (1999) High level of variation at Abies alba chloroplast microsatellite loci in Europe. Mol Ecol 8: 1117-1126. doi: 10. 1046/j. 1365-294x. 1999. 00666. x.
85. Vendramin GG, Anzidei M, Madaghiele A, Sperisen C, Bucci G (2000) Chloroplast microsatellite analysis reveals the presence of population subdivision in Norway spruce (Picea abies K.). Genome 43: 68-78. doi: 10. 1139/gen-43-1-68.
86. Villagran C (1991) Historia de los bosques templados del sur de Chile durante el Tardiglacial y Postglacial. Rev Chil Hist Nat 64: 447-460.
87. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84: 9054-9058. doi: 10. 1073/pnas. 84. 24. 9054.
88. Xu X, Peng M, Xu X (2000) The direction of microsatellite mutations is dependent upon allele length. Nat Genet 24: 396-399. doi: 10. 1038/74238.
89. Young A, Boyle T (2000) Forest fragmentation. In: Young A, Boshier D, Boyle T (eds) Forest conservation genetics. Principles and practice. CSIRO Publishing-CABI Publishing, United Kingdom, pp 123-134.
90. Ziegenhagen B, Scholz F, Madaghiele A, Vendramin GG (1997) Chloroplast microsatellites as markers for paternity analysis in Abies alba. Can J For Res 28: 317-321. doi: 10. 1139/cjfr-28-2-317.