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

Relict islands of the temperate rainforest tree Aextoxicon punctatum (Aextoxicaceae) in semi-arid Chile: genetic diversity and biogeographic history

Mariela C. Núñez-Ávila A B C D and Juan J. Armesto A C
+ Author Affiliations
- Author Affiliations

A CMEB, Laboratorio de Ecología Forestal, Facultad de Ciencias, Universidad de Chile, Santiago, Chile.

B Present address: Instituto de Silvicultura, Universidad Austral de Chile, Valdivia, Chile.

C CASEB, Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile.

D Corresponding author. Email: marielanunez@uach.cl

Australian Journal of Botany 54(8) 733-743 https://doi.org/10.1071/BT06022
Submitted: 8 February 2006  Accepted: 10 July 2006   Published: 29 November 2006

Abstract

Aextoxicon punctatum, the only representative of the family Aextoxicaceae, is a tree species endemic to temperate forests of western South America. This species exhibits a disjunct distribution pattern, with few isolated populations occurring on coastal hilltops of the Chilean semi-arid zone (SAZ), 30–32°S; small populations mixed with sclerophyllous forest in some gorges of the central Chilean Mediterranean coastal range (MCR), 32–39°S; more continuous forests extended along the southern temperate coastal range (TCR), 39–43°S; and fragmented populations eastward in the south temperate central depression and Andean foothills (TAF), 39–41°S. This geographic disjunction is the result of climatic and tectonic changes that took place in southern South America since the late Tertiary, leading to the isolation of forest fragments in the SAZ from the rest of the distribution. According to palynological evidence, populations of TCR and TAF originated from postglacial population expansions from refuges located on the coastal range, north of 40°S. We examined how the present genetic structure and diversity of Aextoxicon populations in Chile reflects this biogeographic history. Random amplified polymorphic DNA (RAPD) markers were used to characterise genetic differences within and among 16 populations of this species throughout its natural range. AMOVA and UPGMA analysis showed high genetic differentiation between the geographically closer SAZ and MCR populations, suggesting a long history of restricted genetic exchange between populations in these two zones. Estimates of Shannon’s genetic diversity and percentage polymorphism were relatively low compared with other southern temperate forest trees (mainly conifers) that were less affected by the glaciations. Positive correlations between genetic and geographic distances were found for TCR but not for TAF populations, suggesting earlier postglacial population expansion southwards along the TCR and more recent eastward migration from coastal locations to TAF during the Holocene.


Acknowledgments

We dedicate this paper to our colleague Carolina Villagrán, who introduced us to the enigmatic history of Olivillo forests and stimulated us to pursue this study. We thank many friends and colleagues for helping with field sampling. Pete Hollingsworth, Adrian Newton, Richard Ennos, Sylvain Fulgeiron, Mark Hershkovitz and Elie Poulin offered technical advice and comments on earlier versions of this manuscript. CONAF and landowners are thanked for allowing access to research sites. This work was supported by graduate fellowships from CMEB (P99-103F-ICM) and from Universidad de Chile (PG/28/02), and by grants from FONDAP-FONDECYT 1501-0001 (CASEB, Pontificia Universidad Católica de Chile) and BIOCORES Project funded by EC under INCO IV program (contract ICA 4-CT-2001-10095). This is a contribution to the research program of Senda Darwin Biological Station, Chile.


References


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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Allnutt TR, Courtis JR, Gardner M, Newton AC (2001) Genetic variation and wild Chilean and cultivated British populations of Podocarpus salignus D.Don (Podocarpaceae). Edinburgh Journal of Botany 58, 459–473. open url image1

Allnutt TR, Newton AC, Premoli AC, Lara A (2003) Genetic variation in the threatened South American conifer Pilgerodendron uviferum (Cupressaceae), detected using RAPD markers. Biological Conservation 114, 245–253.
Crossref | GoogleScholarGoogle Scholar | open url image1

Antonovics J (1968) Evolution in closely adjacent populations. VI. Manifold effects of gene flow. Heredity 23, 507–524. open url image1

Armesto JJ , Aravena JC , Villagrán C , Pérez C , Parker GG (1996) Bosques templados de la Cordillera de la Costa. In ‘Ecología de Los Bosques Nativos de Chile’. (Eds JJ Armesto, C Villagrán, MT Kalin Arroyo) pp. 199–213. (Editorial Universitaria: Santiago, Chile).

Armesto JJ, Rozzi R, Smith-Ramirez C, Arroyo MTK (1998) Conservation targets in South American temperate forests. Science 282, 1271–1272.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bekessy SA, Allnutt 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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends in Ecology and Evolution 13, 202–205.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bull-Hereñu K, Martínez EA, Squeo FA (2005) Structure and genetic diversity in Colliguaja odorífera Mol. (Euphorbiaceae), a shrub subjected to Pleisto-Holocenic natural perturbations in a Mediterranean South American region. Journal of Biogeography 32, 1129–1138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chase HW, Hills HH (1991) Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40, 215–220.
Crossref | GoogleScholarGoogle Scholar | open url image1

CONAF CONAMA, BIRF, Universidad Austral de Chile, Pontificia Universidad Católica de Chile, Universidad Católica de Temuco (1999) ‘Catastro y evaluación de los recursos vegetacionales nativos de Chile.’ (Informe Nacional con Variables Ambientales: Santiago, Chile)

Dawson IK, Simons AJ, Waugh R, Powell W (1995) Diversity and genetic differentiation among subpopulations of Gliricidia sepium revealed by PCR-based assays. Heredity 74, 10–18.
PubMed |
open url image1

Etisham-Ul-Haq M, Allnutt TR, Smith-Ramírez C, Gardner MF, Armesto JJ, Newton AC (2001) Patterns of genetic variation in and ex situ populations of the threatened Chilean vine Berberidopsis corallina, detected using RAPD markers. Annals of Botany 87, 813–821.
Crossref | GoogleScholarGoogle Scholar | open url image1

Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplogroups: applications to human mitochondrial DNA restriction data. Genetics 131, 479–491.
PubMed |
open url image1

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 81, 231–284.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hinojosa LF, Villagrán C (1997) Historia de los bosques del sur de Sudamerica I: Antecedentes paleobotánicos, geológicos y climáticos del terciario del cono sur de América. Revista Chilena de Historia Natural 70, 225–239. open url image1

Jara P, Squeo FA, Hershkovitz M (2002) Divergencia genética en Drimys (canelo) en Chile, mediante análisis con RAPD. Biological Research 35, R-54. open url image1

Jenny B, Valero-Garcés BL, Villa-Martínez R, Urrutia R, Geyh M, Veit H (2002) Early to Mid-Holecene aridity in central Chile and the southern westerlies: The Laguna Aculeo record (34°S). Quaternary Research 58, 160–170.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kummerow J (1966) Aporte al conocimiento de las condiciones climáticas del bosque de Fray Jorge. Boletín Técnico de la Facultad de Agronomía, Universidad de Chile 24, 21–28. open url image1

Lewontin RC (1972) The apportionment of human diversity. Evolutionary Biology 6, 381–398. open url image1

Looser G (1935) Argumentos botánicos a favor de un cambio de clima en Chile central en tiempos geológicos recientes. Revista Universitaria 20, 843–857. open url image1

Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plants populations. Annual Review of Ecology and Systematics 15, 65–95.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Molecular Ecology 3, 91–99.
PubMed |
open url image1

Maldonado A, Villagrán C (2002) Paleoenvironmental changes in the semi-arid coast of Chile (32°S) during the last 6200 cal years inferred from a swamp forest pollen records. Quaternary Research 58, 130–138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.
PubMed |
open url image1

Martínez EA, Núñez-Ávila M (2001) Uso de marcadores moleculares para evaluar el estado híbrido de Colliguaja salicifolia. Biological Research 34, R36. open url image1

Miller MP (1997) Tools for population genetic analyses, TFPGA 1.3: a windows programs for the analysis of allozyme and molecular population genetic data. Computer software distributed by author.

Miller MP (1998) AMOVA-PREP 1.01: a program for the preparation of AMOVA input file from dominant-marker raw data. Computer software distributed by author.

Miller MP (1999) Mantel-Strucure 1.0: a program for the detection of population structure trhuogh the use of Mantel tests. Computer software distributed by author.mpm2@nauvax.ucc.nau.edu.

Muñoz C, Pisano E (1947) Estudio de la vegetación y flora de los parques nacionales de Fray Jorge y Talinay. Agricultura Técnica 7, 71–190. open url image1

Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590. open url image1

Newton AC, Allnut T, Gillies AC, Lowe A, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends in Ecology and Evolution 14, 140–145.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nishida M , Nishida H , Ohsawa T (1988) Preliminary notes on the petrified woods from the Tertiary of Cerro Dorotea, Ultima Esperanza, Chile. A Report of the Botanical Survey to Bolivia and Southern Chile (1986–87). Faculty of Science, Chiba University, Japan, 16–25.

Nybom H, Bartish VI (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, 93–114.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pérez C, Villagrán C (1994) Influencias del clima en el cambio florístico, vegetacional y edáfico de lo bosques de ’olivillo‘ (Aextoxicon punctatum R. et Pav.) de la Cordillera de Costa de Chile: implicancias biogeográficas. Revista Chilena de Historia Natural 67, 77–90. open url image1

Philippi F (1884) A visit to the northernmost forest of Chile. Journal of Botany 22, 202–211. open url image1

Rohlf FL (1992) ‘NTSYS-PC: numerical taxonomy and multivariate analysis system.’ (Exeter Software: New York)

Savolainen V, Chase MW, Hoot SB, Morton CM, Soltis DE, Bayer C, Fay MF, De Bruijn AY, Sullivan S, Qiu YL (2000) Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. Systematic Biology 49, 306–362.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Phylogeographic studies in plants: problems and prospects. Molecular Ecology 7, 465–474.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schmithüsen J (1956) Die räumliche Ordnung der chilenischen Vegetation. Bonner Geographische Abhandlungen 17, 1–86. open url image1

Skottsberg C (1984) Apuntes sobre la historia y vegetación de Fray Jorge (Coquimbo, Chile). Acta Horti Gotoburgensis 18, 91–184. open url image1

Smith-Ramírez C (2004) The Chilean coastal range: a vanishing center of biodiversity and endemism in South American temperate forests. Biodiversity and Conservation 13, 373–393.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith-Ramírez C , Armesto J , Rodríguez J , Gutierrez A , Christie D , Núñez-Ávila M (2005) Aextoxicon punctatum, el tique u olivillo. In ‘Biodiversidad, historia y ecología de los bosques costeros de Chile’. (Eds C Smith-Ramírez, JJ Armesto, C Valdovinos) pp. 278–283. (Editorial Universitaria: Santiago, Chile)

Szmidt AE, Wang XR, Lu MZ (1996) Empirical assessment of allozyme and RAPD variation in Pinus sylvestris (L.) using haploid tissue analysis. Heredity 76, 412–420. open url image1

Troncoso AC, Villagrán C, Muñoz M (1980) Una nueva hipótesis acerca del origen y edad del bosque de Fray Jorge (Coquimbo, Chile). Boletín del Museo Nacional de Historia Natural de Chile 37, 117–152. open url image1

del-Val E, Armesto JJ, Barbosa O, Christie DA, Gutiérrez AG, Jones CG, Marquet PA, Weathers KC (2006) Rain forest islands in the Chilean semi-arid region: fog-dependency, ecosystem persistence and tree regeneration. Ecosystems 9, 598–608.
Crossref | GoogleScholarGoogle Scholar | open url image1

Villa-Martínez R, Villagrán C (1997) Historia de la vegetación de los bosques pantanosos de la costa de Chile central durante el Holoceno medio y tardío. Revista Chilena de Historia Natural 7, 391–401. open url image1

Villagrán C (1991) Historia de los bosques templados del sur de Chile durante el tardiglacial y postglacial. Revista Chilena de Historia Natural 64, 447–460. open url image1

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. Revista Chilena de Historia Natural 74, 793–803. open url image1

Villagrán C , Roig F (2004) ’Historia glacial de dos coníferas milenarias: el alerce y el ciprés de las guaitecas.’ (Corporación Nacional Forestal, Región de Los Lagos: Chile).

Villagrán C, Varela J (1990) Palynological evidence for increased aridity on the central Chilean coast during the Holocene. Quaternary Research 34, 198–207.
Crossref | GoogleScholarGoogle Scholar | open url image1

Villagrán C , Armesto JJ , Hinojosa LF , Cuvertino J , Pérez C , Medina C (2004) El enigmático origen del bosque relicto de Fray Jorge. In ‘Historia natural del parque nacional bosque Fray Jorge’. (Eds FA Squeo, JR Gutiérrez, IR Hernández) pp. 3–43. (Ediciones Universidad de La Serena: La Serena).

Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Research 18, 6531–6536.
PubMed |
open url image1

Wolffhügel K (1949) Rätsel der Notohylaea. Revista Sudamericana de Botánica 8, 45–58. open url image1