Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Multiple Pleistocene refugia in the widespread Patagonian tree Embothrium coccineum (Proteaceae)

Romina Vidal-Russell A B , Cintia P. Souto A and Andrea C. Premoli A
+ Author Affiliations
- Author Affiliations

A Laboratorio Ecotono, INIBIOMA (CONICET-Universidad Nacional del Comahue), Quintral 1250, 8400 Bariloche, Río Negro, Argentina.

B Corresponding author. Email: vidalrussell@comahue-conicet.gob.ar

Australian Journal of Botany 59(4) 299-314 https://doi.org/10.1071/BT10303
Submitted: 13 November 2010  Accepted: 23 March 2011   Published: 9 June 2011

Abstract

Embothrium coccineum J.R.Forst. & G.Forst is an endemic tree of the Patagonian temperate forest. The objective of this study is to evaluate the impact of last glaciation events on the genetic structure of this widespread and ecologically tolerant species, to postulate possible refugial areas. Phylogeographic analyses were performed using chloroplast DNA sequences (trnL-trnF spacer and ndhC-trnV spacer) from individuals collected in 34 populations along the total range of the species, and these results were compared with a similar study in Nothofagus. A total of 22 haplotypes were found, three of which were widely distributed while 13 were found at only one location. Historical demography suggests a long period of stable effective population size, decreasing gradually towards the Last Glacial Maximum (LGM), followed by an increase in population size that stabilised 2500 years ago. The phylogeographic analyses reflect recent events of colonisation after the LGM from multiple refugia. In the northern area of its distribution probably the species survived in several pockets within the Andes mountain range and in Cordillera de la Costa in Chile. In the south, it is suggested that Embothrium survived the glacial period at the edge of the glaciers. These findings are in agreement with the fossil pollen record that shows 10 000-year-old grains in the south, suggesting colonisation from nearby areas when ice retreated. Embothrium is a coloniser that naturally occurs as scattered individuals within mixed forests. Hence, the shallow phylogeographic structure reported here reflects a Pleistocene signature highly impacted by drift resulting in the randomly fixation of new variants reducing the cpDNA structure.


References

Acosta MC, Premoli A (2010) Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Molecular Phylogenetics and Evolution 54, 235–242.
Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae).Crossref | GoogleScholarGoogle Scholar | 19683588PubMed |

Alberdi M, Donoso C (2004) Variabilidad en Embothrium coccineum. In ‘Variación intraespecífica en las especies arbóreas de los bosques templados de Chile y Argentina’. (Eds M Alberdi, C Donoso, A Premoli, L Gallo, R Ipinza) pp. 345–355. (Editorial Universitaria, S. A.: Santiago de Chile)

Allnutt TR, Newton AC, Lara A, Premoli A, Armesto JJ, Vergara R, Gardner M (1999) Genetic variation in Fitzroya cupressoides (alerce), a threatened South American conifer. Molecular Ecology 8, 975–987.
Genetic variation in Fitzroya cupressoides (alerce), a threatened South American conifer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzmtlalsA%3D%3D&md5=064f4b7db1b387949b66fc7d3ee0a430CAS | 10434418PubMed |

Allnutt T, Newton A, Premoli A, Lara A (2003) Genetic variation in the threatened South American conifer Pilgerodendron uviferum (Cupressaceae), detected using RAPD markers. Biological Conservation 114, 245–253.
Genetic variation in the threatened South American conifer Pilgerodendron uviferum (Cupressaceae), detected using RAPD markers.Crossref | GoogleScholarGoogle Scholar |

Amico G, Nickrent D (2009) Population structure and phylogeography of the mistletoes Tristerix corymbosus and T. aphyllus (Loranthaceae) using chloroplast DNA sequence variation. American Journal of Botany 96, 1571–1580.
Population structure and phylogeography of the mistletoes Tristerix corymbosus and T. aphyllus (Loranthaceae) using chloroplast DNA sequence variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2iurzK&md5=a85d64595621ddeda2809190a3ae7120CAS | 21628301PubMed |

Azpilicueta M, Marchelli P, Gallo L (2009) The effects of Quaternary glaciations in Patagonia as evidenced by chloroplast DNA phylogeography of Southern beech Nothofagus obliqua. Tree Genetics & Genomes 5, 561–571.
The effects of Quaternary glaciations in Patagonia as evidenced by chloroplast DNA phylogeography of Southern beech Nothofagus obliqua.Crossref | GoogleScholarGoogle Scholar |

Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.

Barker NP, Weston PH, Rutschmann F, Sauquet H (2007) Molecular dating of the ‘Gondwanan’ plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana. Journal of Biogeography 34, 2012–2027.
Molecular dating of the ‘Gondwanan’ plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana.Crossref | GoogleScholarGoogle Scholar |

Bekessy S, Allnutt T, Premoli A, Lara A, Ennos R, Burgman M, Cortes M, Newton A (2002) Genetic variation in the vulnerable and endemic Monkey Puzzle tree, detected using RAPDs. Heredity 88, 243–249.
Genetic variation in the vulnerable and endemic Monkey Puzzle tree, detected using RAPDs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs1Kju7c%3D&md5=f5b36d5c4b2075c306a9630ea423456dCAS | 11920130PubMed |

Castro-Arévalo M, Reyes-Díaz M, Alberdi M, Jara-rodríguez V, Sanhueza C, Corcuera LJ, Bravo LA (2008) Effects of low temperature acclimation on photosynthesis in three Chilean Proteaceae. Revista Chilena de Historia Natural (Valparaiso, Chile) 81, 321–333.
Effects of low temperature acclimation on photosynthesis in three Chilean Proteaceae.Crossref | GoogleScholarGoogle Scholar |

Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples. Version 8. (Persistent URL purl.oclc.org/estimates (accessed 13 January 2011)

Cosacov A, Sérsic AN, Sosa V, Johnson LA, Cocucci AA (2010) Multiple periglacial refugia in the Patagonian steppe and post glacial colonization of the Andes: the phylogeography of Calceolaria polyrhiza. Journal of Biogeography 37, 1463–1477.

Devoto M, Montaldo NH, Medan D (2006) Mixed hummingbird: long-proboscid-fly pollination in ornithophilous Embothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia, Argentina. Austral Ecology 31, 512–519.
Mixed hummingbird: long-proboscid-fly pollination in ornithophilous Embothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |

Drummond A, Rambaut A, Shapiro B, Pybus O (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22, 1185–1192.
Bayesian coalescent inference of past population dynamics from molecular sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVKitb4%3D&md5=ce36aa7afe931999ffb5c52c2af4a537CAS | 15703244PubMed |

Dumolin-Lapegue S, Pemonge M, Petit R (1997) An enlarged set of consensus primers for the study of organelle DNA in plants. Molecular Ecology 6, 393–397.
An enlarged set of consensus primers for the study of organelle DNA in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVOhurY%3D&md5=58e97cb8c473cd464084101d6f34a26cCAS | 9131816PubMed |

Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571–2581.
A simulated annealing approach to define the genetic structure of populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nptlaksw%3D%3D&md5=ad39f5aeb9fd6520bf1edce73fd2c073CAS | 12453240PubMed |

Escobar BR, Donoso C, Souto CP, Alberdi M, Zúñiga A (2006) Embothrium coccineum. In ‘Las especies arbóreas de los bosques templados de Chile y Argentina. Autoecología’. (Ed. C Donoso) pp. 233–243. (Marisa Cuneo: Valdivia)

Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47

Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368–376.
Evolutionary trees from DNA sequences: a maximum likelihood approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXls1Cisr8%3D&md5=1a56dd2bb731f74d46d5e6866bccfaadCAS | 7288891PubMed |

Fesq-Martin M, Friedmann A, Peters M, Behrmann J, Kilian R (2004) Late-glacial and Holocene vegetation history of the Magellanic rain forest in southwestern Patagonia, Chile. Vegetation History and Archaeobotany 13, 249–255.
Late-glacial and Holocene vegetation history of the Magellanic rain forest in southwestern Patagonia, Chile.Crossref | GoogleScholarGoogle Scholar |

Fu Y (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.

Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

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. Geografiska Annaler. Series A. Physical Geography 81, 231–284.
Paleoecology of the southern Chilean Lake District-Isla Grande de Chiloé during middle-late Llanquihue glaciation and deglaciation.Crossref | GoogleScholarGoogle Scholar |

Heusser CJ, Heusser LE, Lowell TV (2000) Deglacial palaeoclimate at Puerto del Hambre, subantarctic Patagonia, Chile. Journal of Quaternary Science 15, 101–114.
Deglacial palaeoclimate at Puerto del Hambre, subantarctic Patagonia, Chile.Crossref | GoogleScholarGoogle Scholar |

Hewitt G, Ibrahim K (2001) Inferring glacial refugia and historical migrations with molecular phylogenies. Special Publication – British Ecologial Society 14, 271–294.

Jakob S, Martinez-Meyer E, Blattner F (2009) Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. Molecular Biology and Evolution 26, 907–923.
Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Clurg%3D&md5=7cd835ccac849dfbbf14f3ebb6ceb82cCAS | 19168565PubMed |

Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service version 3.16. BMC Genetics 6, 13. Available at http://ibdws.sdsu.edu/ [Accessed 26 March 2010]. 10.1186/1471-2156-6-13

Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=f14e7bcbd8917e201f38819e83664a74CAS | 19346325PubMed |

Marchelli P, Gallo LA (2004) The combined role of glaciation and hybridization in shaping the distribution of genetic variation in a Patagonian southern beech. Journal of Biogeography 31, 451–460.
The combined role of glaciation and hybridization in shaping the distribution of genetic variation in a Patagonian southern beech.Crossref | GoogleScholarGoogle Scholar |

Marchelli P, Gallo L (2006) Multiple ice-age refugia in a southern beech of South America as evidenced by chloroplast DNA markers. Conservation Genetics 7, 591–603.
Multiple ice-age refugia in a southern beech of South America as evidenced by chloroplast DNA markers.Crossref | GoogleScholarGoogle Scholar |

Marchelli P, Baier C, Mengel C, Ziegenhagen B, Gallo L (2010) Biogeographic history of the threatened species Araucaria araucana (Molina) K. Koch and implications for conservation: a case study with organelle DNA markers. Conservation Genetics 11, 951–963.

Markgraf V, McGlone M, Hope G (1995) Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective. Trends in Ecology & Evolution 10, 143–147.
Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFajug%3D%3D&md5=03e5768339126358dcab11ba5e54d867CAS | 21236983PubMed |

Mathiasen P, Premoli A (2010) Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America. Molecular Ecology 19, 371–385.
Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOntLY%3D&md5=5cf44353b8d12566142570d5efd33f82CAS | 20002584PubMed |

Mathiasen P, Rovere AE, Premoli AC (2007) Genetic structure and early effects of inbreeding in fragmented temperate forests of a self-incompatible tree, Embothrium coccineum. Conservation Biology 21, 232–240.
Genetic structure and early effects of inbreeding in fragmented temperate forests of a self-incompatible tree, Embothrium coccineum.Crossref | GoogleScholarGoogle Scholar | 17298529PubMed |

Muellner A, Tremetsberger K, Stuessy T, Baeza C (2005) Pleistocene refugia and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae). Molecular Ecology 14, 203–212.
Pleistocene refugia and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2FhvVykug%3D%3D&md5=907044e2d4314dfd5db91733cb522b43CAS | 15643964PubMed |

Pastorino M, Gallo L (2002) Quaternary evolutionary history of Austrocedrus chilensis, a cypress native to the Andean Patagonian forest. Journal of Biogeography 29, 1167–1178.
Quaternary evolutionary history of Austrocedrus chilensis, a cypress native to the Andean Patagonian forest.Crossref | GoogleScholarGoogle Scholar |

Pastorino M, Marchelli P, Milleron M, Soliani C, Gallo L (2009) The effect of different glaciation patterns over the current genetic structure of the southern beech Nothofagus antarctica. Genetica 136, 79–88.
The effect of different glaciation patterns over the current genetic structure of the southern beech Nothofagus antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFejur0%3D&md5=45183fcb053e8925a4541872f6da0581CAS | 18758967PubMed |

Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14, 817–818.
MODELTEST: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=8ebcc96fe364afb58d0db53f65540072CAS | 9918953PubMed |

Premoli AC (1998) The use of genetic markers to conserve endangered species and to design protected areas of more widespread species. In ‘Proceedings International Workshop: Recent Advances in Biotechnology for Tree Conservation and Management’. (Ed. IFF Science) pp. 157–171. (Universidade Federal de Santa Catarina: Florianópolis)

Premoli A, Kitzberger T, Veblen T (2000) Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides. Journal of Biogeography 27, 251–260.
Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides.Crossref | GoogleScholarGoogle Scholar |

Premoli A, Souto C, Rovere A, Allnut T, Newton A (2002) Patterns of isozyme variation as indicators of biogeographic history in Pilgerodendron uviferum (D. Don) Florin. Diversity & Distributions 8, 57–66.
Patterns of isozyme variation as indicators of biogeographic history in Pilgerodendron uviferum (D. Don) Florin.Crossref | GoogleScholarGoogle Scholar |

Premoli AC, Mathiasen P, Kitzberger T (2010) Southernmost Nothofagus trees enduring ice ages: genetic evidence and ecological niche retrodiction reveal high latitude (54°S) glacial refugia. Palaeogeography, Palaeoclimatology, Palaeoecology 285, 186–193.
Southernmost Nothofagus trees enduring ice ages: genetic evidence and ecological niche retrodiction reveal high latitude (54°S) glacial refugia.Crossref | GoogleScholarGoogle Scholar |

Quiroga M, Premoli A (2010) Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events. Palaeogeography, Palaeoclimatology, Palaeoecology 285, 186–193.
Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events.Crossref | GoogleScholarGoogle Scholar |

Rabassa J, Coronato AM, Salemme M (2005) Chronology of the Late Cenozoic Patagonian glaciations and their correlation with biostratigraphic units of the Pampean region (Argentina). Journal of South American Earth Sciences 20, 81–103.
Chronology of the Late Cenozoic Patagonian glaciations and their correlation with biostratigraphic units of the Pampean region (Argentina).Crossref | GoogleScholarGoogle Scholar |

Rodriguez RR, Matthei SO, Quezada MM (1983) ‘Flora arborea de Chile.’ (Editorial de la Universidad de Concepción: Concepción)

Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=ce052ef7410c48193c0097d7e345d0d5CAS | 12912839PubMed |

Rovere AE, Smith-Ramirez C, Armesto JJ, Premoli AC (2006) Breeding system of Embothrium coccineum (Proteaceae) in two populations on different slopes of the Andes. Revista Chilena de Historia Natural (Valparaiso, Chile) 79, 225–232.
Breeding system of Embothrium coccineum (Proteaceae) in two populations on different slopes of the Andes.Crossref | GoogleScholarGoogle Scholar |

Ruiz E, Gonzalez F, Torres-Diaz C, Fuentes G, Mardones M, Stuessy T, Samuel R, Becerra J, Silva M (2007) Genetic diversity and differentiation within and among Chilean populations of Araucaria araucana (Araucariaceae) based on allozyme variability. Taxon 56, 1221–1228.
Genetic diversity and differentiation within and among Chilean populations of Araucaria araucana (Araucariaceae) based on allozyme variability.Crossref | GoogleScholarGoogle Scholar |

Sauquet H, Weston PH, Anderson CL, Barker NP, Cantrill DJ, Mast AR, Savolainen V (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proceedings of the National Academy of Sciences of the United States of America 106, 221–225.
Contrasted patterns of hyperdiversification in Mediterranean hotspots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltF2ksw%3D%3D&md5=3d0751cd70b55b72e4a7df08b9d1360bCAS | 19116275PubMed |

Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94, 275–288.
Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFOjsLg%3D&md5=3e1a3dffb1bf631a8f5de29620fe09e9CAS | 21636401PubMed |

Smith-Ramírez C, Rovere AE, Núñez-Ávila MC, Armesto JJ (2007) Habitat fragmentation and reproductive ecology of Embothrium coccineum, Eucryphia cordifolia and Aextoxicon punctatum. In ‘Biodiversity loss and conservation in fragmented forest landscapes: the forests of montane Mexico and temperate South America’. (Ed. AC Newton) pp. 102–119. (CABI: Wallingford)

Souto C, Premoli A (2007) Genetic variation in the widespread Embothrium coccineum (Proteaceae) endemic to Patagonia: effects of phylogeny and historical events. Australian Journal of Botany 55, 809–817.
Genetic variation in the widespread Embothrium coccineum (Proteaceae) endemic to Patagonia: effects of phylogeny and historical events.Crossref | GoogleScholarGoogle Scholar |

Steubing L, Alberdi M, Wenzel H (1983) Seasonal changes of cold resistance of Proteaceae of the South Chilean laurel forest. Plant Ecology 52, 35–44.

Swofford DL (2003) PAUP* 4.0 b10. Phylogenetic analysis using parsimony (* and other methods). (Sinauer Associates: Sunderland, MA)

Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
Universal primers for amplification of three non-coding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhslel&md5=881be45efb56742ff78711a8a4bdb4cfCAS | 1932684PubMed |

Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.

Tortorelli LA (1956) ‘Maderas y bosques argentinos.’ (Editorial Acme, SACI: Buenos Aires) 910 pp.

Wenzens G (2002) The influence of tectonically derived relief and climate on the extent of the last Glaciation east of the Patagonian ice fields (Argentina, Chile). Tectonophysics 345, 329–344.
The influence of tectonically derived relief and climate on the extent of the last Glaciation east of the Patagonian ice fields (Argentina, Chile).Crossref | GoogleScholarGoogle Scholar |

Wolfe K, Li W, Sharp P (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United States of America 84, 9054–9058.
Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXovVyktQ%3D%3D&md5=803622971b2d487758f334c7f5ff5c52CAS | 3480529PubMed |