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

Unravelling the evolutionary history of Eucalyptus cordata (Myrtaceae) using molecular markers

Peter A. Harrison A B , Rebecca C. Jones A , René E. Vaillancourt A , Robert J. E. Wiltshire A and Brad M. Potts A

A School of Biological Sciences and National Centre for Future Forest Industries, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.

B Corresponding author. Email: P.A.Harrison@utas.edu.au

Australian Journal of Botany 62(2) 114-131 http://dx.doi.org/10.1071/BT14019
Submitted: 6 February 2014  Accepted: 16 March 2014   Published: 5 May 2014

Abstract

We studied the evolutionary processes shaping the genetic diversity in the naturally fragmented Eucalyptus cordata, a rare homoblastic tree endemic to the island of Tasmania. A genome-wide scan showed that E. cordata and the endangered heteroblastic E. morrisbyi were closely related, suggesting a neotenous origin of E. cordata from an endemic heteroblastic ancestor. Bayesian cluster analysis based on nuclear microsatellites assayed in 567 E. cordata and E. morrisbyi individuals revealed five genetic clusters. Two clusters comprised populations that correspond to putative ancestral gene pools linking E. cordata and E. morrisbyi. Another cluster included populations that transgressed the drowned Derwent River valley, suggestive of a wider glacial distribution. However, the majority of individuals occurred in the two genetic clusters distributed in the south-west and north-east of the range of E. cordata. The elevated genetic diversity in populations comprising these clusters suggests that they represent two recently fragmented cores of the distribution. Genetic evidence suggests that the newly described, localised E. cordata subspecies quadrangulosa has been recently selected from within the morphologically diverse, south-western cluster. We argue that multiple phases of isolation and drift have led to the contemporary pattern of molecular variation and the scattering of relictual and more recently derived populations across the species distribution.

Additional keywords: Diversity Array Technology (DArT), Eucalyptus, gene flow, genetic drift, heteroblastic, homoblastic, microsatellite, spatial genetic structuring.


References

Arnold ML, Martin NH (2009) Adaptation by introgression. Journal of Biology 8, 82.1–82.3.
Adaptation by introgression.CrossRef | open url image1

Bloomfield JA, Nevill P, Potts BM, Vaillancourt RE, Steane DA (2011) 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 | open url image1

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 | 1:CAS:528:DyaK1cXotVaht7o%3D&md5=37cef8a5ff1ad21a5b1896c6127dd08dCAS | open url image1

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,
A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus.CrossRef | open url image1

Brooker MIH (2000) A new classification of the genus Eucalyptus L’Her. (Myrtaceae). Australian Systematic Botany 13, 79–148.
A new classification of the genus Eucalyptus L’Her. (Myrtaceae).CrossRef | open url image1

Brussard PF (1984) Geographic patterns and environmental gradients: the central–marginal model in Drosophila revisited. Annual Review of Ecology and Systematics 15, 25–64.
Geographic patterns and environmental gradients: the central–marginal model in Drosophila revisited.CrossRef | open url image1

Buschbom J, Yanbaev Y, Degen B (2011) Efficient long-distance gene flow into an isolated relict oak stand. The Journal of Heredity 102, 464–472.
Efficient long-distance gene flow into an isolated relict oak stand.CrossRef | 21525180PubMed | open url image1

Butcher PA, Otero A, McDonald MW, Moran GF (2002) Nuclear RFLP variation in Eucalyptus camaldulensis Dehnh. from northern Australia. Heredity 88, 402–412.
Nuclear RFLP variation in Eucalyptus camaldulensis Dehnh. from northern Australia.CrossRef | 1:CAS:528:DC%2BD38XksFSrs70%3D&md5=daf02295e3582a23d6ac4bda5187a0beCAS | 11986878PubMed | open url image1

Butcher PA, Skinner AK, Gardiner CA (2005) Increased inbreeding and inter-species gene flow in remnant populations of the rare Eucalyptus benthamii. Conservation Genetics 6, 213–226.
Increased inbreeding and inter-species gene flow in remnant populations of the rare Eucalyptus benthamii.CrossRef | open url image1

Byrne M (2008) Phylogeny, diversity and evolution of eucalypts. In ‘Plant genome. Biodiversity and evolution. Vol. 1’. (Eds AK Sharma, A Sharma) pp. 303–346. (Science Publishers: Plymouth, UK)

Byrne M, Hopper SD (2008) Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia. Biological Journal of the Linnean Society. Linnean Society of London 93, 177–188.
Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia.CrossRef | open url image1

Byrne M, Moran GF, Tibbits WN (1993) Restriction map and maternal inheritance of chloroplast DNA in Eucalyptus nitens. The Journal of Heredity 84, 218–220.

Canestrelli D, Aloise G, Cecchetti S, Nascetti G (2010) Birth of a hotspot of intraspecific genetic diversity: notes from the underground. Molecular Ecology 19, 5432–5451.
Birth of a hotspot of intraspecific genetic diversity: notes from the underground.CrossRef | 21059127PubMed | open url image1

Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. The Journal of Heredity 100, 106–113.
Simultaneous estimation of null alleles and inbreeding coefficients.CrossRef | 1:CAS:528:DC%2BD1MXhtVKmsA%3D%3D&md5=9c239e6f48faf049b2f6a61e64629a16CAS | 18936113PubMed | open url image1

Comps B, Gomory D, Letouzey J, Thiebaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157, 389–397.

Cremer KW (1977) Distance of seed dispersal in Eucalyptus estimated from seed weights. Australian Forest Research 7, 225–228.

Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12, 13–15.

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 | open url image1

Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Molecular Ecology 17, 1170–1188.
Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond.CrossRef | 1:CAS:528:DC%2BD1cXksFShsbc%3D&md5=4d56d481228082e84adcec7cdff7ef25CAS | 18302683PubMed | open url image1

Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24, 217–242.
Population genetic consequences of small population size: implications for plant conservation.CrossRef | open url image1

Ennos RA (1994) Estimating the relative rates of pollen and peed migration among plant-populations. Heredity 72, 250–259.
Estimating the relative rates of pollen and peed migration among plant-populations.CrossRef | open url image1

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 | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=9768cb9d92ec62dae4e93a84977410f8CAS | 15969739PubMed | open url image1

Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annual Review of Ecology Evolution and Systematics 40, 481–501.
Genetic consequences of range expansions.CrossRef | open url image1

Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.

Field DL, Ayre DJ, Whelan RJ, Young AG (2009) Molecular and morphological evidence of natural interspecific hybridization between the uncommon Eucalyptus aggregata and the widespread E. rubida and E. viminalis. Conservation Genetics 10, 881–896.
Molecular and morphological evidence of natural interspecific hybridization between the uncommon Eucalyptus aggregata and the widespread E. rubida and E. viminalis.CrossRef | 1:CAS:528:DC%2BD1MXntlShurc%3D&md5=91f2d2a92ecad0d8e3e657a6f62227aaCAS | open url image1

Freeman JS, Jackson HD, Steane DA, McKinnon GE, Dutkowski GW, 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 | 1:CAS:528:DC%2BD3MXptVemu7w%3D&md5=000698299ba2aece477203fb156d7086CAS | open url image1

Goudet J (2002) ‘FSTAT, a program to estimate and test gene diversities and fixation indices. Version 2.9.3.’ (Department of Ecology & Evolution, UNIL: Lausanne, Switzerland). Available at http://www2.unil.ch/popgen/softwares/fstat.htm.[Verified 3 April 2014]

Hampe A, Pemonge MH, Petit RJ (2013) Efficient mitigation of founder effects during the establishment of a leading-edge oak population. Proceedings. Biological Sciences 280,
Efficient mitigation of founder effects during the establishment of a leading-edge oak population.CrossRef | open url image1

Hudson CJ, Freeman JS, Kullan ARK, Petroli CD, Sansaloni CP, Kilian A, Dettering F, Grattapaglia D, Potts BM, Myburg AA, Vaillancourt RE (2012) A reference linkage map for Eucalyptus. BMC Genomics 13, 240
A reference linkage map for Eucalyptus.CrossRef | 1:CAS:528:DC%2BC38Xhslamu7zM&md5=d587321f71f6633511e37f4b06bd3d51CAS | 22702473PubMed | open url image1

Jackson WD (2005) Palaeohistory of vegetation change: the last 2 million years. In ‘Vegetation of Tasmania’. (Eds JB Reid, RS Hill, MJ Brown, MJ Hovenden) pp. 64–88. (Australian Biological Resources Study: Hobart)

Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.CrossRef | 1:CAS:528:DC%2BD2sXpt1ahtbs%3D&md5=8ee17ac13abf31e1c79922b4db068da5CAS | 17485429PubMed | open url image1

Jones RC, McKinnon GE, Potts BM, Vaillancourt RE (2005) Genetic diversity and mating system of an endangered tree Eucalyptus morrisbyi. Australian Journal of Botany 53, 367–377.
Genetic diversity and mating system of an endangered tree Eucalyptus morrisbyi.CrossRef | open url image1

Jones RC, Steane DA, Lavery M, Vaillancourt RE, Potts BM (2013) Multiple evolutionary processes drive the patterns of genetic differentiation in a forest tree species complex. Ecology and Evolution 3, 1–17.
Multiple evolutionary processes drive the patterns of genetic differentiation in a forest tree species complex.CrossRef | open url image1

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 | open url image1

Klier K, Leoschke MJ, Wendel JF (1991) Hybridisation and interogression in white and yellow ladyslipper orchards (Cypripedium candidum and C. pubescens). The Journal of Heredity 82, 305–319.

Larcombe M, Barbour RC, Vaillancourt RE, Potts BM (2014) Assessing the risk of exotic gene flow from Eucalyptus globulus plantations to native E. ovata forests. Forest Ecology and Management 312, 193–202.
Assessing the risk of exotic gene flow from Eucalyptus globulus plantations to native E. ovata forests.CrossRef | open url image1

Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? Journal of Ecology 94, 942–952.
How general are positive relationships between plant population size, fitness and genetic variation?CrossRef | open url image1

Lewis PO, Zaykin D (2001) ‘Genetic data analysis: computer program for the analysis of allelic data. Version 1.1.’ Available at http://www.eeb.uconn.edu/people/plewis/software.php.[Verified 3 April 2014]

Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111, 675–689.

McKinnon GE, Vaillancourt RE, Jackson HD, Potts BM (2001a) Chloroplast sharing in the Tasmanian eucalypts. Evolution 55, 703–711.
Chloroplast sharing in the Tasmanian eucalypts.CrossRef | 1:CAS:528:DC%2BD3MXktleqtLs%3D&md5=2d9ad781175a1e23995a1b774aa8bd0bCAS | 11392388PubMed | open url image1

McKinnon GE, Vaillancourt RE, Tilyard PA, Potts BM (2001b) Maternal inheritance of the chloroplast genome in Eucalyptus globulus and interspecific hybrids. Genome 44, 831–835.
Maternal inheritance of the chloroplast genome in Eucalyptus globulus and interspecific hybrids.CrossRef | 1:CAS:528:DC%2BD3MXos12ls78%3D&md5=acd2c803322f37c4dbe34be37dc99044CAS | open url image1

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 | 15101583PubMed | open url image1

McKinnon GE, Vaillancourt RE, Steane DA, Potts BM (2004b) The rare silver gum, Eucalyptus cordata, is leaving its traces in the organellar gene pool of Eucalyptus globulus. Molecular Ecology 13, 3751–3762.
The rare silver gum, Eucalyptus cordata, is leaving its traces in the organellar gene pool of Eucalyptus globulus.CrossRef | 15548288PubMed | open url image1

McKinnon GE, Vaillancourt RE, Steane DA, Potts BM (2008) An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae). American Journal of Botany 95, 368–380.
An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae).CrossRef | 1:CAS:528:DC%2BD1cXktlyjs7Y%3D&md5=0eb70a7c44c6ee79b3bb4f96a51d319bCAS | 21632361PubMed | open url image1

McKinnon GE, Smith JJ, Potts BM (2010) Recurrent nuclear DNA introgression accompanies chloroplast DNA exchange between two eucalypt species. Molecular Ecology 19, 1367–1380.
Recurrent nuclear DNA introgression accompanies chloroplast DNA exchange between two eucalypt species.CrossRef | 1:CAS:528:DC%2BC3cXlvVWhtrk%3D&md5=7c565fd5e2471b50431348cd63665b2dCAS | 20298471PubMed | open url image1

Nei M (1972) Genetic distance between populations. American Naturalist 106, 283
Genetic distance between populations.CrossRef | open url image1

Nei H (1987) ‘Molecular evolution genetics.’ (Columbia University Press: New York)

Nicolle D (2006) ‘Eucalypts of Victoria and Tasmania.’ (Bloomings Books: Melbourne)

Nicolle D, Potts BM, McKinnon GE (2008) Eucalyptus cordata subsp. quadrangulosa (Myrtaceae), a new taxon of restricted distribution from Southern Tasmania. In ‘Papers and proceedings of the Royal Society of Tasmania. No. 142, Vol. 2’. pp. 71–78. (The Royal Society of Tasmania: Hobart)

Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537–2539.
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update.CrossRef | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=039b7447ba51da3cb7b5b5ad3760bb54CAS | 22820204PubMed | open url image1

Petit RJ, Kremer A, Wagner DB (1993) Finite island model for organelle and nuclear genes in plants. Heredity 71, 630–641.
Finite island model for organelle and nuclear genes in plants.CrossRef | open url image1

Potts BM (1988) The distribution and type locality of Eucalyptus cordata Labill. – an historical account. In ‘Papers and proceedings of the Royal Society of Tasmania. No. 122, Vol. 2‘. pp. 31–38. (The Royal Society of Tasmania: Hobart)

Potts BM (1989) ‘Population variation and conservation status of a rare Tasmanian endemic, Eucalyptus cordata.’ (Tasmanian Forest Research Council: Hobart)

Potts BM, Wiltshire RJE (1997) Eucalypt genetics and genecology. In ‘Eucalypt ecology: individuals to ecosystems’. (Eds JE Williams, JCZ Woinarski) pp. 56–91. (Cambridge University Press: New York)

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

R Core Team (2012) ‘R: a language and environment for statistical computing. Version 2.15.1.’ (The R Foundation for Statistical Computing, Institute for Statistics and Mathematics: Vienna). Available at http://cran.r-project.org/.[Verified 3 April 2014]

Rathbone DA, McKinnon GE, Potts BM, Steane DA, Vaillancourt RE (2007) Microsatellite and cpDNA variation in island and mainland populations of a regionally rare eucalypt, Eucalyptus perriniana (Myrtaceae). Australian Journal of Botany 55, 513–520.
Microsatellite and cpDNA variation in island and mainland populations of a regionally rare eucalypt, Eucalyptus perriniana (Myrtaceae).CrossRef | 1:CAS:528:DC%2BD2sXpt1SltbY%3D&md5=0bbb12ba830fdcab3edf544d2a266f44CAS | open url image1

Rieseberg LH, Kim SC, Randell RA, Whitney KD, Gross BL, Lexer C, Clay K (2007) Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129, 149–165.
Hybridization and the colonization of novel habitats by annual sunflowers.CrossRef | 16955330PubMed | open url image1

Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.

Sansaloni CP, Petroli CD, Jaccoud D, Carling J, Detering F, Grattapaglia D, Kilian A (2011) Diversity Arrays Technology (DArT) and next generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proceedings 5, 54–55.
Diversity Arrays Technology (DArT) and next generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus.CrossRef | open url image1

Slee AV, Brooker MIH, Duffy SM, West JG (2006) ‘EUCLID: eucalypts of Australia.’ 3rd edn (CSIRO Publishing: Melbourne)

Smith S, Hughes J, Wardell-Johnson G (2003) High population differentiation and extensive clonality in a rare mallee eucalypt: Eucalyptus curtisii – conservation genetics of a rare mallee eucalypt. Conservation Genetics 4, 289–300.

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, Nicolle D, Sansaloni CP, Petroli CD, Carling J, Kilian A, Myburg AA, Grattapaglia D, Vaillancourt RE (2011) Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping. Molecular Phylogenetics and Evolution 59, 206–224.
Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping.CrossRef | 21310251PubMed | open url image1

Threatened Species Unit (2003) ‘Morrisby’s gum, Eucalyptus morrisbyi draft flora recovery plan, 2004–2008.’ (Department of Primary Industries, Water and Environment: Hobart)

Tyson M, Vaillancourt RE, Reid JB (1998) Determination of clone size and age in a mallee eucalypt using RAPDs. Australian Journal of Botany 46, 161–172.
Determination of clone size and age in a mallee eucalypt using RAPDs.CrossRef | 1:CAS:528:DyaK1cXksV2qurk%3D&md5=7728a74c3e2380866ac6091a2d470d35CAS | open url image1

Vekemans X (2010) What’s good for you may be good for me: evidence for adaptive introgression of multiple traits in wild sunflower. New Phytologist 187, 6–9.
What’s good for you may be good for me: evidence for adaptive introgression of multiple traits in wild sunflower.CrossRef | 20624229PubMed | open url image1

Vucetich JA, Waite TA (2003) Spatial patterns of demography and genetic processes across the species’ range: null hypotheses for landscape conservation genetics. Conservation Genetics 4, 639–645.
Spatial patterns of demography and genetic processes across the species’ range: null hypotheses for landscape conservation genetics.CrossRef | open url image1

Whitney KD, Randell RA, Rieseberg LH (2010) Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytologist 187, 230–239.
Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus.CrossRef | 20345635PubMed | open url image1

Williams K, Potts M (1996) The natural distribution of Eucalyptus species in Tasmania. Tasforests 8, 39–149.

Wiltshire RJE, Potts BM, Reid JB (1991) Phenotypic affinities, variability and conservation status of a rare Tasmanian endemic, Eucalyptus morrisbyi R.G.Brett. In ‘Aspects of Tasmanian botany – a tribute to Winifred Curtis’. (Eds MR Banks, SJ Smith, AE Orchard, G Gantvilas) pp. 213–229. (Royal Society of Tasmania: Hobart)

Woodhams M, Steane DA, Jones RC, Nicolle D, Moulton V, Holland BR (2013) Novel distances for Dollo data. Systematic Biology 62, 62–77.
Novel distances for Dollo data.CrossRef | 22914977PubMed | open url image1

Yatabe Y, Kane NC, Scotti-Saintagne C, Rieseberg LH (2007) Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175, 1883–1893.
Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris.CrossRef | 1:CAS:528:DC%2BD2sXmsFyls7w%3D&md5=2ee98812bbe15a684e663d250f0466dcCAS | 17277373PubMed | open url image1


Full Text PDF (2.31 MB) Export Citation