Abstract
Climatic oscillations during the Quaternary strongly affected the distribution of warm-temperate tree species, which experienced local restrictions into ice-free areas and posterior expansions. To evaluate the impact of these range movements on the genetic structure of populations, we performed a phylogeographical analysis of the species Nothofagus obliqua with chloroplast DNA markers. A total of 27 populations covering the whole natural distribution range were analyzed using polymerase chain reaction-restriction fragment length polymorphism. Diversity (h T, h S), allelic richness (r g), and differentiation among populations for unordered (G ST) and ordered alleles (N ST) were calculated. The relationships among haplotypes were evaluated by the construction of a minimum spanning network. The spatial distribution of the genetic variation was analyzed through a Mantel test and with a nested analysis of molecular variance to differentiate between geographic regions. The screening of 11 non-coding regions allowed the identification of 14 haplotypes. A high genetic differentiation was detected (N ST = 0.875 and G ST = 0.824) with the existence of phylogeographic structure (p < 0.05). The distribution of the genetic variation was partially explained by the topography of the region when the populations were divided longitudinally into Coastal Mountains, Central Valley, and Andes Mountains (ϕ RT = 0.093, p = 0.001). In agreement with pollen records, our results support the hypothesis of Coastal refuges since the region harbors high diversity together with older and private haplotypes. Long-lasting persistence of some Coastal populations without contribution to re-colonization is proposed. Additional refuges are also postulated along the Andes and Longitudinal Valley. Survival in multiple glacial refuges is discussed together with the possible migratory routes.
Similar content being viewed by others
References
Allnut TR, Newton AC, Premoli A, Lara A (2003) Genetic variation in the threatened South American conifer Pilgerodendron uviferum (Cupressaceae), detected using RAPD markers. Biol Conserv 114:245–253
Auer V (1958) The Pleistocene of Fuego-Patagonia. Auer V (1958) The Pleistocene of Fuego-Patagonia. Ann Acad Sci Fenn, A 3 50:1–239
Bekessy SA, Allnut TR, Premoli AC, Lara A, Ennos RA, Burgman MA, Cortes M, Newton AC (2002) Genetic variation in the vulnerable and endemic Monkey Puzzle tree, detected using RAPDs. Heredity 88:243–249
Bennet KD, Haberle SG, Lumley SH (2000) The Last Glacial-Holocene transition in southern Chile. Science 290:325–328
Bordács S, Popescu F, Slade D et al (2002) Chloroplast DNA variation of white oaks in northern Balkans and in the Carpathian Basin. For Ecol Manag 156:197–209
Comps B, Gömöry D, Letouzey J, Thiébaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397
Demesure B, Sodzi N, Petit RJ (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
Demesure B, Comps B, Petit RJ (1996) Chloroplast DNA phylogeography of the common beech (Fagus sylvatica L.) in Europe. Evolution 50(6):2515–2520
Donoso C (1993) Bosques templados de Chile y Argentina. Variación, estructura y dinámica. Ecología forestal. Editorial Universitaria, Chile
Dumolin S, Demesure B, Petit RJ (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91:1253–1256
Dumolin-Lapegue S, Pemonge MH, Petit RJ (1997a) An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 146:1475–1487
Dumolin-Lapegue S, Demesure B, Fineschi S, Le Corre V, Petit RJ (1997b) Geographic structure of white oaks throughout the European continent. Genetics 146:1475–1487
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839
Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136:343–359
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Flint RF, Fidalgo F (1964) Glacial geology of the East flank of the Argentine Andes between latitude 39º 10’ S and latitude 41° 20′ S. Geol Soc Am Bull 75:335–352
Gallo LA (2002) Conceptual and experimental elements to model natural inter-specific hybridisation between two mountain southern beeches (Nothofagus spp.). In: Degen B, Loveless MD, Kremer A (eds) Modelling and experimental research on genetic processes in tropical and temperate forests. Embrapa-Silvolab, Guyane
Gallo L, Marchelli P, Crego P, Oudkerk L, Breitembücher A, Peñalba M, Chauchard L, Maresca L y Cuerpo de Guardaparques PN Lanín y Nahuel Haupi (2000) Distribución y variación genética en características seminales y adaptativas de poblaciones y progenies de Raulí en Argentina. In: Ipinza Carmona R, Gutiérrez Caro B, Emhart Schmidt V (eds) Domesticación y mejora genética de raulí y roble. Valdivia, Chile
Gallo LA, Marchelli P, Pastorino MJ, Azpilicueta MM (2008) Fragmentación y reclusión: una teoría para explicar el patrón de variación filogeográfica de numerosas especies arbóreas. Basic and Applied Genetics XIX:198
Grivet D, Heinze B, Vendramin GG, Petit RJ (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 1(4):345–349
Grivet D, Deguilloux M-F, Petit RJ, Sork VL (2006) Contrasting patterns of historical colonization in white oaks (Quercus spp.) in California and Europe. Mol Ecol 15(13):4085–4093
Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forest 6:95–124
Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 14:393–412
Heinze B (2007) A database of PCR primers for the chloroplast genomes of higher plants. Plant Methods 3:4
Heusser CJ (1983) Quaternary pollen record from Laguna de Tagua Tagua, Chile. Science 219:1429–1432
Heusser CJ (1984) Late-Glacial-Holocene climate of Lake District of Chile. Quat Res 22:77–90
Heusser CJ, Heusser LE, Lowell TV (1999) Paleoecology of the southern Chilean lake district-Isla Grande de Chiloé during middle-late Llanquihue glaciation and deglaciation. Geogr Ann 81A:231–284
Kodama KP, Rabassa J, Evenson EB, Clinch JM (1986) Paleomagnetismo y edad relative del drift Pichileufu en su área tipo, San Carlos de Bariloche, Río Negro. Asoc Geol Argent XLI:165–178
Magri D, Vendramin GG, Comps B et al (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171(1):199–221
Mantel N (1967) The detection of disease and a generalized regression approach. Cancer Res 27(2):209–220
Marchelli P, Gallo LA (2004) The combined role of glaciation and hybridization in shaping the distribution of the genetic variation in a Patagonian southern beech. J Biogeogr 31:1–10
Marchelli P, Gallo LA (2006) Multiple ice-age refugia in a southern beech of South America as evidenced by chloroplast DNA markers. Conserv Genet 7:591–603
Marchelli P, Gallo L, Scholz F, Ziegenhagen B (1998) Chloroplast DNA markers reveal a geographical divide across Argentinean southern beech Nothofagus nervosa (Phil.) Dim. et Mil. distribution area. Theor Appl Genet 97:642–646
Markgraf V (1987) Paleoenvironmental changes at the Northern limit of the Subantarctic Nothofagus forests, lat. 37°S, Argentina. Quatern Res 28:119–129
Markgraf V (1991) Late Pleistocene environmental and climatic evolution in southern South America. Bamb Geogr Schr 11:271–281
Markgraf V, McGlone M, Hope G (1995) Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems—a southern perspective. Trends Ecol Evol 10:143–147
Markgraf V, Romero EJ, Villagrán C (1996) History and paleoecology of South American Nothofagus forests. In: Veblen TT (ed) The ecology and biogeography of Nothofagus forests. Yale University Press, New Haven & London, pp 354–386
Milleron M, Gallo LA, Marchelli P (2008) The effect of volcanism on postglacial migration and seed dispersal. A case study in southern South America. Tree Genetics and Genomes . doi:10.1007/s11295-007-0121-1
Moreno P (1997) Vegetation and climate near Lago Llanquihue in the Chilean Lake district between 20200 and 9500 14C yr BP. J Quat Sci 12:485–500
Muellner AN, Tremetsberger K, Stuessy T, Baeza CM (2005) Pleistocene and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae). Mol Ecol 14:203–212
Palmé AE, Su Q, Rautenberg A, Manni F, Lascoux M (2003) Postglacial recolonization and cpDNA variation of silver birch, Betula pendula. Mol Ecol 12:201–212
Pastorino MJ, Gallo LA (2002) Quaternary evolutionary history of Austrocedrus chilensis, a cypress native to the Andean-Patagonian forest. J Biogeogr 29:1167–1178
Pastorino MJ, Marchelli P, Milleron M, Soliani C, Gallo LA (2008) The effect of different glaciation patterns over the current genetic structure of the southern beech Nothofagus antarctica. Genetica . doi:10.1007/s10709-008-9314-2
Peakall R, Smouse PE (2005) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research. Australian National University, Canberra, Australia. http://www.anu.edu.au/BoZo/GenAlEx/
Petit RJ, Vendramin GG (2006) Plant phylogeography based on organelle genes: an introduction. In: Weiss S, Ferrand N (eds) Phylogeography of southern European refugia. Evolutionary perspectives on the origins and conservation of European biodiversity. Springer, New York, pp 23–97
Petit RJ, Kremer A, Wagner DB (1993) Geographic structure of chloroplast DNA polymorphism in European oaks. Theor Appl Genet 87:122–128
Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci U S A 94:9996–10001
Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565
Peyron O, Guiot J, Cheddadi R (1998) Chloroplast DNA footsprints of postglacial recolonisation by oaks. Proc Natl Acad Sci U S A 94:9996–10001
Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity I. Haploid locus. Theor Appl Genet 90:462–470
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered and unordered alleles. Genetics 144:1237–1245
Premoli A, Kitzberger T, Veblen TT (2000) Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides. J Biogeogr 27:251–260
Rabassa J, Clapperton CM (1990) Quaternary glaciations in the southern Andes. Quat Sci Rev 9:153–174
Romero-Severson J, Aldrich P, Feng Y, Sun W, Michler C (2003) Chloroplast DNA variation of northern red oak (Quercus rubra L.) in Indiana. New Forest 26:43–49
Souza-Chies TT, Bittar G, Nadot S, Carter L, Besin E, Lejeune B (1997) Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Syst Evol 204:109–123
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
Veit H, Garleff K (1996) Evolución del paisaje cuaternario y los suelos en Chile central-sur. In: Armesto JJ, Villagrán C, Arroyo MK (eds) Ecología de los bosques nativos de Chile. Editorial Universitaria, Santiago de Chile, Chile, pp 29–49
Villagrán C (1991) Historia de los bosques templados del sur de Chile durante el Tardiglacial y Postglacial. Rev Chil Hist Nat 64:447–460
Villagrán C (2001) Un modelo de la historia de la vegetación de la Cordillera de la Costa de Chile central-sur: la hipótesis glacial de Darwin. Rev Chil Hist Nat 74(4):793–803
Villagrán C, Moreno P, Villa R (1996) Antecedentes palinológicos acerca de la historia cuaternaria de los bosques chilenos. In: Armesto JJ, Villagrán C, Arroyo MK (eds) Ecología de los bosques nativos de Chile. Editorial Universitaria, Santiago de Chile, Chile, pp 51–69
Villagrán C, Le-Quesne C, Aravena JC, Jiménez H, Hinojosa F (1998) El rol de los cambios de clima del cuaternario en la distribución actual de la vegetación de Chile central-sur. Bamb Geogr Schr 15:227–242
Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19
Widmer A, Lexer C (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 16(6):267–269
Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058
Acknowledgments
The authors would like to thank Carolina Soliani for her helpful laboratory assistance. We are grateful to Lucas Oudkerk, Fernanda Izquierdo, Liliana Lozano, and Lanin National Park rangers who helped in sample collection within Argentinean populations. Viviana Becerra and Mario Paredes from INIA Quilamapu, Chile provided the seeds from populations in Chile. Chilean geographical locations were provided by Braulio Gutiérrez from INFOR, Chile. The study was supported by the project “Genetic characterization of populations of N. obliqua (Mirb. et Oerst.) and N. nervosa ((Phil.) Dim. et Mil. through molecular and isozymes markers” BID-FONTAGRO-IICA, between INIA Quilamapu, Chile and INTA Bariloche, Argentina. We are grateful for the valuable comments made by three anonymous reviewers which contributed to improve the manuscript. Paula Marchelli is a researcher from CONICET.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Vendramin
Rights and permissions
About this article
Cite this article
Azpilicueta, M.M., Marchelli, P. & Gallo, L.A. The effects of Quaternary glaciations in Patagonia as evidenced by chloroplast DNA phylogeography of Southern beech Nothofagus obliqua . Tree Genetics & Genomes 5, 561–571 (2009). https://doi.org/10.1007/s11295-009-0209-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-009-0209-x