Molecular genetic diversity and population structure in Eucalyptus pauciflora subsp. pauciflora (Myrtaceae) on the island of Tasmania
Archana Gauli A C , Dorothy A. Steane A B , René E. Vaillancourt A and Brad M. Potts AA School of Biological Sciences and National Centre for Future Forest Industries, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.
B Faculty of Science, Health, Education and Engineering and Collaborative Research Network, University of the Sunshine Coast, Locked Bag 4, Maroochydore, Qld 4558, Australia.
C Corresponding author. Email: Archana.Gauli@utas.edu.au
Australian Journal of Botany 62(3) 175-188 https://doi.org/10.1071/BT14036
Submitted: 23 February 2014 Accepted: 18 May 2014 Published: 27 June 2014
Abstract
Genetic diversity and population structure of Tasmanian populations of Eucalyptus pauciflora were assessed using chloroplast and nuclear microsatellite markers. Maternal trees and open-pollinated progeny from 37 populations were sampled across the species’ geographic and altitudinal distribution in Tasmania. The distribution of chloroplast haplotype richness showed a clear geographic structure with suggestion of three major refugia (Storm Bay, Tamar Valley and St Pauls River Valley), two of which are consistent with previously reported glacial refugia. Chloroplast haplotype affinities provided evidence of migration of populations from the north and east towards the south and west of Tasmania. High nuclear microsatellite diversity was observed across the species’ range. Most of this variation was distributed within populations with low but significant FST, suggesting high gene flow among populations that is more pronounced in mature stands. Higher nuclear genetic diversity in newly colonised areas compared with lowland putative refugial regions, and the converse in chloroplast DNA markers, suggest limited seed dispersal into newly colonised regions combined with high pollen flow between different source populations in newly colonised areas. Our results do not support the suggestion that highland populations of E. pauciflora originate from in situ high-altitude refugia, but instead argue they originate from lowland refugia.
Additional keywords: Eucalyptus pauciflora, genetic diversity, haplotypes, molecular markers, spatial structure.
References
Austerlitz F, Mariette S, Machon N, Gouyon P-H, Godelle B (2000) Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154, 1309–1321.Bailey T, Davidson N, Potts B, Gauli A, Hovenden M, Burgess S, Duddles J (2013) Plantings for carbon, biodiversity and restoration in dry rural landscapes. Australian Forest Grower 35, 39–41.
Baillie PW (1989) Jurassic–Cainozoic. In ‘Geology and mineral resources of Tasmania’. (Eds CR Burrett, EL Martin) pp. 339–409. (Geological Society of Australia: Melbourne)
Bloomfield JA, Nevill P, Potts BM, Vaillancourt RE, Steane DA (2011a) Molecular genetic variation in a widespread forest tree species Eucalyptus obliqua (Myrtaceae) on the island of Tasmania. Australian Journal of Botany 59, 226–237.
| Molecular genetic variation in a widespread forest tree species Eucalyptus obliqua (Myrtaceae) on the island of Tasmania.Crossref | GoogleScholarGoogle Scholar |
Bloomfield JA, Nevill P, Vaillancourt RE, Steane DA, Potts BM (2011b) Stringy bark diversity study winds up: new data on genetic diversity in Eucalyptus obliqua on the island of Tasmania. In ‘Biobuzz. Vol. 15’. (CRC for Forestry: Hobart) Available at http://www.crcforestry.com.au/view/index71dc.html?id=81972. [Accessed 20 February 2014]
Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM, Johnston RD, Kleinig DA, Turner JD (2002) ‘Forest trees of Australia.’ (CSIRO: Canberra)
Brondani RPV, Brondani C, Tarchini R, Grattapaglia D (1998) Development, characterization and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla. Theoretical and Applied Genetics 97, 816–827.
| Development, characterization and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVaht7o%3D&md5=37cef8a5ff1ad21a5b1896c6127dd08dCAS |
Brondani RPV, Williams ER, Brondani C, Grattapaglia D (2006) A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus. BMC Plant Biology 6, 20
| A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus.Crossref | GoogleScholarGoogle Scholar |
Byrne M (2008) Phylogeny, diversity and evolution of eucalypts. In ‘Plant genome: biodiversity and evolution. Vol. 1. Part E. Phanerogams–Angiosperm’. (Eds AK Sharma, A Sharma) pp. 303–346. (Science Publishers: Berlin, Germany)
Byrne M, Parrish TL, Moran GF (1998) Nuclear RFLP diversity in Eucalyptus nitens. Heredity 81, 225–233.
| Nuclear RFLP diversity in Eucalyptus nitens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVaktLo%3D&md5=e4bfaf91c14712c6efcc8c1f80b096fcCAS |
Demesure B, Comps B, Petit RJ (1996) Chloroplast DNA phylogeography of the common beech (Fagus sylvatica L.) in Europe. Evolution 50, 2515–2520.
| Chloroplast DNA phylogeography of the common beech (Fagus sylvatica L.) in Europe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFamtw%3D%3D&md5=1027099830ed59f09ca54afa182ca94bCAS |
Dodson J (1977) Late Quaternary palaeoecology of Wyrie Swamp, southeastern South Australia. Quaternary Research 8, 97–114.
| Late Quaternary palaeoecology of Wyrie Swamp, southeastern South Australia.Crossref | GoogleScholarGoogle Scholar |
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12, 13–15.
Duncan F (1989) Systematic affinities, hybridisation and clinal variation within Tasmanian eucalypts. Tasforests 2, 13–26.
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
| STRUCTURE HARVESTER: a website and program for visualizing structure output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |
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. Theoretical and Applied Genetics 92, 832–839.
| High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L) Skeels] endemic to Morocco.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7gs1answ%3D%3D&md5=a046e6d5566579fe42d3e0f4d6d89488CAS | 24166548PubMed |
Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72, 250–259.
| Estimating the relative rates of pollen and seed migration among plant populations.Crossref | GoogleScholarGoogle Scholar |
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=9768cb9d92ec62dae4e93a84977410f8CAS | 15969739PubMed |
Ferris C, King RA, Väinölä R, Hewitt GM (1998) Chloroplast DNA recognizes three refugial sources of European oaks and suggests independent eastern and western immigrations to Finland. Heredity 80, 584–593.
| Chloroplast DNA recognizes three refugial sources of European oaks and suggests independent eastern and western immigrations to Finland.Crossref | GoogleScholarGoogle Scholar | 9650279PubMed |
Finkeldey R, Mátyás G (2003) Genetic variation of oaks (Quercus spp.) in Switzerland. 3. Lack of impact of postglacial recolonization history on nuclear gene loci. Theoretical and Applied Genetics 106, 346–352.
Freeman JS, Jackson HD, Steane DA, McKinnon GE, Potts BM, Vaillancourt RE (2001) Chloroplast DNA phylogeography of Eucalyptus globulus. Australian Journal of Botany 49, 585–596.
| Chloroplast DNA phylogeography of Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVemu7w%3D&md5=000698299ba2aece477203fb156d7086CAS |
Gauli A, Vaillancourt RE, Steane DA, Bailey TG, Potts BM (2014) The effect of forest fragmentation and altitude on the mating system of Eucalyptus pauciflora (Myrtaceae). Australian Journal of Botany 61, 622–632.
| The effect of forest fragmentation and altitude on the mating system of Eucalyptus pauciflora (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Glaubitz JC, Emebiri LC, Moran GF (2001) Dinucleotide microsatellites from Eucalyptus sieberi: inheritance, diversity, and improved scoring of single-based differences. Genome 44, 1041–1045.
| Dinucleotide microsatellites from Eucalyptus sieberi: inheritance, diversity, and improved scoring of single-based differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvVOgug%3D%3D&md5=b27fdb3e4ac1ce6d94d4c455f250c7cbCAS | 11768207PubMed |
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. Version 2.9.3. Available at http://www.unil.ch/izea/softwares/fstat.html. [Accessed 20 July 2013]
Hardner CM, Potts BM (1997) Post-dispersal selection under mixed-mating in Eucalyptus regnans. Evolution 51, 103–111.
| Post-dispersal selection under mixed-mating in Eucalyptus regnans.Crossref | GoogleScholarGoogle Scholar |
Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Frascaria-Lacoste N, Hardy OJ, Vekemans X, Vendramin GG (2004) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Molecular Ecology 13, 3437–3452.
| Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWkurjE&md5=cbc4f6bf0b981eebd12152ef828c21a2CAS | 15488002PubMed |
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society. Linnean Society of London 58, 247–276.
| Some genetic consequences of ice ages, and their role in divergence and speciation.Crossref | GoogleScholarGoogle Scholar |
Hope GS, Kirkpatrick JB (1989) The ecological history of Australian forests. In ‘Australia’s ever-changing forests’. (Eds K Frawley, N Semple) pp. 3–22. (University College, ADFA: Canberra)
House SM (1997) Reproductive biology of eucalypts. In ‘Eucalypt ecology: individuals to ecosystems’. (Eds J Williams, JCZ Woinarski) pp. 30–55. (Cambridge University Press: Cambridge, UK)
Hufford KM, Hamrick JL (2003) Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution 57, 518–526.
| Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae).Crossref | GoogleScholarGoogle Scholar | 12703941PubMed |
Jones RC, Steane DA, Potts BM, Vaillancourt RE (2002) Microsatellite and morphological analysis of Eucalyptus globulus populations. Canadian Journal of Forest Research 32, 59–66.
| Microsatellite and morphological analysis of Eucalyptus globulus populations.Crossref | GoogleScholarGoogle Scholar |
Jones TH, Vaillancourt RE, Potts BM (2007) Detection and visualization of spatial genetic structure in continuous Eucalyptus globulus forest. Molecular Ecology 16, 697–707.
| Detection and visualization of spatial genetic structure in continuous Eucalyptus globulus forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1Gmu7k%3D&md5=85c7ab5b48084a6089d9e57c35529619CAS | 17284205PubMed |
Kirkpatrick JB, Brown MJ (1984) The palaeogeographic significance of local endemism in Tasmanian higher plants. Search 15, 112–113.
Kirkpatrick JB, Fowler M (1998) Locating likely glacial forest refugia in Tasmania using palynological and ecological information to test alternative climatic models. Biological Conservation 85, 171–182.
| Locating likely glacial forest refugia in Tasmania using palynological and ecological information to test alternative climatic models.Crossref | GoogleScholarGoogle Scholar |
Kremer A, Petit RJ, Stephan BR, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, König AO, Lowe AJ, Munro RC (2002) Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks? Forest Ecology and Management 156, 75–87.
| Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks?Crossref | GoogleScholarGoogle Scholar |
Lewis PO, Zaykin D (2002) Genetic data analysis: computer program for the analysis of allelic data. Version 1.1. Available at http://lewis.eeb.uconn.edu/lewishome/software.html. [Accessed 20 July 2013]
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.
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. Theoretical and Applied Genetics 97, 642–646.
| Chloroplast DNA markers reveal a geographical divide across Argentinean southern beech Nothofagus nervosa (Phil.) Dim. et Mil. distribution area.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFOgt74%3D&md5=14629a224aec9bdc7a0a237c1d0bb04cCAS |
McKinnon GE, Vaillancourt RE, Jackson HD, Potts BM (2001) Chloroplast sharing in the Tasmanian eucalypts. Evolution 55, 703–711.
| Chloroplast sharing in the Tasmanian eucalypts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktleqtLs%3D&md5=2d9ad781175a1e23995a1b774aa8bd0bCAS | 11392388PubMed |
McKinnon GE, Jordan GJ, Vaillancourt RE, Steane DA, Potts BM (2004a) Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 275–284.
| Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts.Crossref | GoogleScholarGoogle Scholar | 15101583PubMed |
McKinnon GE, Vaillancourt RE, Steane DA, Potts BM (2004b) The rare silver gum, Eucalyptus cordata, is leaving its trace in the organellar gene pool of Eucalyptus globulus. Molecular Ecology 13, 3751–3762.
| The rare silver gum, Eucalyptus cordata, is leaving its trace in the organellar gene pool of Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar | 15548288PubMed |
Naito Y, Konuma A, Iwata H, Suyama Y, Seiwa K, Okuda T, Lee SL, Muhammad N, Tsumura Y (2005) Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae). Journal of Plant Research 118, 423–430.
| Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae).Crossref | GoogleScholarGoogle Scholar | 16283070PubMed |
Nei M (1972) Genetic distance between populations. American Naturalist 106, 283–292.
| Genetic distance between populations.Crossref | GoogleScholarGoogle Scholar |
Nevill P (2010) ‘Genetic variation in Eucalyptus regnans F.Muell.’ (The University of Melbourne: Melbourne)
Nevill PG, Bossinger G, Ades PK (2010) Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia. Journal of Biogeography 37, 179–192.
| Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia.Crossref | GoogleScholarGoogle Scholar |
Newton AC, Allnutt TR, Gillies ACM, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends in Ecology & Evolution 14, 140–145.
| Molecular phylogeography, intraspecific variation and the conservation of tree species.Crossref | GoogleScholarGoogle Scholar |
Nicolle D (2006) ‘Eucalypts of Victoria and Tasmania.’ (Bloomings Books: Melbourne)
Ottewell KM, Donnellan SC, Moran GF, Paton DC (2005) Multiplexed microsatellite markers for the genetic analysis of Eucalyptus leucoxylon (Myrtaceae) and their utility for ecological and breeding studies in other Eucalyptus species. The Journal of Heredity 96, 445–451.
| Multiplexed microsatellite markers for the genetic analysis of Eucalyptus leucoxylon (Myrtaceae) and their utility for ecological and breeding studies in other Eucalyptus species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsV2iu7c%3D&md5=d6517e65efc6985e7c25925abc6d0e6aCAS | 15843635PubMed |
Patterson B, Wolbang CM, Vaillancourt RE, Potts BM (2000) Inheritance of two chlorophyll mutants in Eucalyptus globulus. Silvae Genetica 49, 290–292.
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proceedings of the National Academy of Sciences, USA 94, 9996–10001.
| Chloroplast DNA footprints of postglacial recolonization by oaks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvVWmtb4%3D&md5=a172e6fc1d1e761a548424b21559cf4eCAS |
Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12, 844–855.
| Identifying populations for conservation on the basis of genetic markers.Crossref | GoogleScholarGoogle Scholar |
Petit RJ, Csaikl UM, Bordács S, Burg K, Coart E, Cottrell J, van Dam B, Deans JD, Dumolin-Lapègue S, Fineschi S, Finkeldey R, Gillies A, Glaz I, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Olalde M, Pemonge M-H, Popescu F, Slade D, Tabbener H, Taurchini D, de Vries SGM, Ziegenhagen B, Kremer A (2002a) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecology and Management 156, 5–26.
| Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations.Crossref | GoogleScholarGoogle Scholar |
Petit RJ, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Brewer S, Mátyás G, Munro RC, Popescu F, Slade D, Tabbener H, de Vries SGM, Ziegenhagen B, de Beaulieu J-L, Kremer A, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van Dam B (2002b) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecology and Management 156, 49–74.
| Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence.Crossref | GoogleScholarGoogle Scholar |
Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14, 689–701.
| Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVGitrw%3D&md5=c3f847b84a34a50d5b3faecae5333113CAS | 15723661PubMed |
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237–1245.
Potts BM, Reid JB (1985) Variation in the Eucalyptus gunnii-archeri complex. II. The origin of variation. Australian Journal of Botany 33, 519–541.
| Variation in the Eucalyptus gunnii-archeri complex. II. The origin of variation.Crossref | GoogleScholarGoogle Scholar |
Potts B, Wiltshire R (1997) Eucalypt genetics and genecology. In ‘Eucalypt ecology: individuals to ecosystems’. (Eds JE Williams, JCZ Woinarski) pp. 56–91. (Cambridge University Press: Cambridge, UK)
Premoli AC, Kitzberger T, Veblen TT (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 |
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Pryor LD 1951
Pryor LD 1953
Ritland K (2002) Extensions of models for the estimation of mating systems using an independent loci. Heredity 88, 221–228.
| Extensions of models for the estimation of mating systems using an independent loci.Crossref | GoogleScholarGoogle Scholar | 11920127PubMed |
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
| GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar | 21585727PubMed |
Schneeweiss GM, Schonswetter P (2011) A re-appraisal of nunatak survival in arctic-alpine phylogeography. Molecular Ecology 20, 190–192.
| A re-appraisal of nunatak survival in arctic-alpine phylogeography.Crossref | GoogleScholarGoogle Scholar | 21265053PubMed |
Shepherd M, Sexton TR, Thomas D, Henson M, Henry RJ (2010) Geographical and historical determinants of microsatellite variation in Eucalyptus pilularis. Canadian Journal of Forest Research 40, 1051–1063.
| Geographical and historical determinants of microsatellite variation in Eucalyptus pilularis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtVKjsLk%3D&md5=e8f57b082dce79db5ad32ad8c834f12bCAS |
Sigleo WR Colhoun EA 1981
Skabo S, Vaillancourt RE, Potts BM (1998) Fine-scale genetic structure of Eucalyptus globulus ssp globulus forest revealed by RAPDs. Australian Journal of Botany 46, 583–594.
| Fine-scale genetic structure of Eucalyptus globulus ssp globulus forest revealed by RAPDs.Crossref | GoogleScholarGoogle Scholar |
Steane DA, Vaillancourt RE, Russell J, Powell W, Marshall D, Potts BM (2001) Development and characterisation of microsatellite loci in Eucalyptus globulus (Myrtaceae). Silvae Genetica 50, 89–91.
Steane DA, Jones RC, Vaillancourt RE (2005) A set of chloroplast microsatellite primers for Eucalyptus (Myrtaceae). Molecular Ecology Notes 5, 538–541.
| A set of chloroplast microsatellite primers for Eucalyptus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOhtbvJ&md5=f1481e49b02db9ce621951e25e4025c9CAS |
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
| Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |
Williams JE (1991) Biogeographic patterns of three sub-alpine eucalypts in south-east Australia with special reference to Eucalyptus pauciflora Sieb. ex Spreng. Journal of Biogeography 18, 223–230.
| Biogeographic patterns of three sub-alpine eucalypts in south-east Australia with special reference to Eucalyptus pauciflora Sieb. ex Spreng.Crossref | GoogleScholarGoogle Scholar |
Williams J, Ladiges PY (1985) Morphological variation in Victorian, lowland populations of Eucalyptus pauciflora Sieb.ex Spreng. Proceedings of the Royal Society of Victoria 97, 31–48.
Williams KJ, Potts BM (1996) The natural distribution of Eucalyptus species in Tasmania. Tasforests 8, 39–165.
Yeoh SH, Bell JC, Foley WJ, Wallis IR, Moran GF (2012) Estimating population boundaries using regional and local-scale spatial genetic structure: an example in Eucalyptus globulus. Tree Genetics & Genomes 8, 695–708.
| Estimating population boundaries using regional and local-scale spatial genetic structure: an example in Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |