Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

Genetic diversity and differentiation in south-western Australian bloodwoods (Corymbia section Calophyllae, Myrtaceae) with different ranges and abundance

Jane Sampson A , Sarah Tapper A , David Coates A , Margaret Hankinson A , Shelley McArthur A and Margaret Byrne https://orcid.org/0000-0002-7197-5409 A *
+ Author Affiliations
- Author Affiliations

A Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, Perth, WA 6983, Australia.

* Correspondence to: margaret.byrne@dbca.wa.gov.au

Handling Editor: Susan Hoebee

Australian Journal of Botany 70(2) 146-157 https://doi.org/10.1071/BT21081
Submitted: 4 July 2021  Accepted: 20 December 2021   Published: 16 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

An understanding of how variation is shared within and among closely related species is important for understanding evolutionary processes and managing biological diversity. We studied genetic structure in the three species occurring in south-western Australia that form the small and distinct monophyletic section Calophyllae of the genus Corymbia. We compared diversity in nuclear microsatellites and chloroplast DNA sequences in two species with patchy distributions, namely, Corymbia haematoxylon (Maiden) K.D. Hill & L.A.S. Johnson and Corymbia ficifolia (F. Muell.) K.D. Hill & L.A.S. Johnson, with that in the widespread congener, C. calophylla (Lindl.) K.D. Hill & L.A.S. Johnson. Consistent with predictions for the influence of range and abundance on genetic structure in the Australian flora, population differentiation was higher in the two restricted patchy species than in the widespread, semicontinuous C. calophylla. Genetic diversity in C. haematoxylon was similar to that in C. calophylla, but diversity was lower in the highly localised C. ficifolia, likely owing to genetic bottlenecks. All three species were distinguished by nuclear SSR variation, but C. haematoxylon and C. ficifolia each shared chloroplast haplotypes with C. calophylla from incomplete lineage sorting of ancestral variation and introgression. Limited evidence of recent hybridisation in two populations of C. haematoxylon was also present.

Keywords: bottleneck, differentiation, diversity, expansion, forest tree, hybridisation, inbreeding, lineage sorting, localised range, patchy abundance.


References

Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.
Median-joining networks for inferring intraspecific phylogenies.Crossref | GoogleScholarGoogle Scholar | 10331250PubMed |

Barbour RC, Otahal Y, Vaillancourt RE, Potts BM (2008) Assessing the risk of pollen-mediated gene flow from exotic Eucalyptus globulus plantations into native eucalypt populations of Australia. Biological Conservation 141, 896–907.
Assessing the risk of pollen-mediated gene flow from exotic Eucalyptus globulus plantations into native eucalypt populations of Australia.Crossref | GoogleScholarGoogle Scholar |

Barrett SCH, Harder LD (2017) The ecology of mating and its evolutionary consequences in seed plants. Annual Review of Ecology, Evolution, and Systematics 48, 135–157.
The ecology of mating and its evolutionary consequences in seed plants.Crossref | GoogleScholarGoogle Scholar |

Bayly MJ, Rigault P, Spokevicius A, Ladiges PY, Ades PK, Anderson C, Bossinger G, Merchant A, Udovicic F, Woodrow IE, Tibbits J (2013) Chloroplast genome analysis of Australian eucalypts – Eucalyptus, Corymbia, Angophora, Allosyncarpia and Stockwellia (Myrtaceae). Molecular Phylogenetics and Evolution 69, 704–716.
Chloroplast genome analysis of Australian eucalypts – Eucalyptus, Corymbia, Angophora, Allosyncarpia and Stockwellia (Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 23876290PubMed |

Booth TH (2017) Going nowhere fast: a review of seed dispersal in eucalypts. Australian Journal of Botany 65, 401–410.
Going nowhere fast: a review of seed dispersal in eucalypts.Crossref | GoogleScholarGoogle Scholar |

Bradbury D, Grayling PM, MacDonald B, Hankinson M, Byrne M (2016) Clonality, interspecific hybridisation and inbreeding in a rare mallee eucalypt, Eucalyptus absita (Myrtaceae), and implications for conservation. Conservation Genetics 17, 193–205.
Clonality, interspecific hybridisation and inbreeding in a rare mallee eucalypt, Eucalyptus absita (Myrtaceae), and implications for conservation.Crossref | GoogleScholarGoogle Scholar |

Bradbury D, Binks RM, Byrne M (2021) Genomic data inform conservation of rare tree species: clonality, diversity and hybridity in Eucalyptus series in a global biodiversity hotspot. Biodiversity and Conservation 30, 619–641.
Genomic data inform conservation of rare tree species: clonality, diversity and hybridity in Eucalyptus series in a global biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |

Broadhurst L, Breed M, Lowe A, Bragg J, Catullo R, Coates D, Encinas-Viso F, Gellie N, James E, Krauss S, Potts B, Rossetto M, Shepherd M, Byrne M (2017) Genetic diversity and structure of the Australian flora. Diversity and Distributions 23, 41–52.
Genetic diversity and structure of the Australian flora.Crossref | GoogleScholarGoogle Scholar |

Byrne M (2008) Eucalypt phylogeny, diversity and evolution. In ‘Plant genome: biodiversity and evolution. 1E: phanerogam – angiosperm’. (Eds AK Sharma, A Sharma) pp. 303–346. (Science Publishers: Enfield, NH, USA)

Byrne M, Hankinson M (2012) Testing the variability of chloroplast sequences for plant phylogeography. Molecular Ecology Resources 60, 569–574.
Testing the variability of chloroplast sequences for plant phylogeography.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Elliott CP, Yates CJ, Coates DJ (2008) Maintenance of high pollen dispersal in Eucalyptus wandoo, a dominant tree of the fragmented agricultural region in Western Australia. Conservation Genetics 9, 97–105.
Maintenance of high pollen dispersal in Eucalyptus wandoo, a dominant tree of the fragmented agricultural region in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Coates DJ, Macdonald BM, Hankinson M, McArthur SM, van Leeuwen S (2016) High nuclear genetic differentiation, but low chloroplast diversity in a rare species, Aluta quadrata (Myrtaceae), with a disjunct distribution in the Pilbara, Western Australia. Australian Journal of Botany 64, 687–695.
High nuclear genetic differentiation, but low chloroplast diversity in a rare species, Aluta quadrata (Myrtaceae), with a disjunct distribution in the Pilbara, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.
Microsatellite null alleles and estimation of population differentiation.Crossref | GoogleScholarGoogle Scholar | 17150975PubMed |

Churchill DM (1968) The distribution and prehistory of Eucalyptus diversicolor F.Muell., E. marginata Donn ex SM., and E. calophylla R.Br. in relation to rainfall. Australian Journal of Botany 16, 125–151.
The distribution and prehistory of Eucalyptus diversicolor F.Muell., E. marginata Donn ex SM., and E. calophylla R.Br. in relation to rainfall.Crossref | GoogleScholarGoogle Scholar |

Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62, 1908–1920.
The hidden side of invasions: massive introgression by local genes.Crossref | GoogleScholarGoogle Scholar | 18452573PubMed |

Dieringer D, Schlötterer C (2003) MICROSATELLITE ANALYSER: a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3, 167–169.
MICROSATELLITE ANALYSER: a platform independent analysis tool for large microsatellite data sets.Crossref | GoogleScholarGoogle Scholar |

Dixon CJ, Schönswetter P, Schneeweiss GM (2007) Traces of ancient range shifts in a mountain plant group (Androsace halleri complex, Primulaceae). Molecular Ecology 16, 3890–3901.
Traces of ancient range shifts in a mountain plant group (Androsace halleri complex, Primulaceae).Crossref | GoogleScholarGoogle Scholar | 17850552PubMed |

Drummond AJ, 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 |

Duminil J, Fineschi S, Hampe A, Jordano P, Salvini D, Vendramin GG, Petit RJ (2007) Can population genetic structure be predicted from life-history traits? The American Naturalist 169, 662–672.
Can population genetic structure be predicted from life-history traits?Crossref | GoogleScholarGoogle Scholar | 17427136PubMed |

Edwards CE, Soltis DE, Soltis PS (2008) Using patterns of genetic structure based on microsatellite loci to test hypotheses of current hybridization, ancient hybridization and incomplete lineage sorting in Conradina (Lamiaceae). Molecular Ecology 17, 5157–5174.
Using patterns of genetic structure based on microsatellite loci to test hypotheses of current hybridization, ancient hybridization and incomplete lineage sorting in Conradina (Lamiaceae).Crossref | GoogleScholarGoogle Scholar | 19120994PubMed |

Ellstrand NC (2014) Is gene flow the most important evolutionary force in plants? American Journal of Botany 101, 737–753.
Is gene flow the most important evolutionary force in plants?Crossref | GoogleScholarGoogle Scholar | 24752890PubMed |

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 | 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 | 15969739PubMed |

Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Felsenstein J (1989) PHYLIP – phylogeny inference package (version 3.2). Cladistics 5, 164–166.
PHYLIP – phylogeny inference package (version 3.2).Crossref | GoogleScholarGoogle Scholar |

Field DL, Ayre DJ, Whelan RJ, Young AG (2011) Patterns of hybridization and asymmetrical gene flow in hybrid zones of the rare Eucalyptus aggregata and common E. rubida. Heredity 106, 841–853.
Patterns of hybridization and asymmetrical gene flow in hybrid zones of the rare Eucalyptus aggregata and common E. rubida.Crossref | GoogleScholarGoogle Scholar | 21063438PubMed |

Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection.Crossref | GoogleScholarGoogle Scholar | 9335623PubMed |

Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133, 693–709.
Statistical tests of neutrality of mutations.Crossref | GoogleScholarGoogle Scholar | 8454210PubMed |

Gilbert KJ, Andrew RL, Bock DG, Franklin MT, Kane NC, Moore JS, Moyers BT, Renaut S, Rennison DJ, Veen T, Vines TH (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure. Molecular Ecology 21, 4925–4930.
Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure.Crossref | GoogleScholarGoogle Scholar | 22998190PubMed |

Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. American Journal of Botany 87, 783–792.
Patterns of genetic variation in rare and widespread plant congeners.Crossref | GoogleScholarGoogle Scholar | 10860909PubMed |

González-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr N, Laffan SW, Miller JT, Rosauer DF, Faith DP, Nipperess DA, Kujala H, Linke S, Butt N, Külheim C, Crisp MD, Gruber B (2016) Phylogenetic approaches reveal biodiversity threats under climate change. Nature Climate Change 6, 1110–1114.
Phylogenetic approaches reveal biodiversity threats under climate change.Crossref | GoogleScholarGoogle Scholar |

Healey A, Lee DJ, Furtado A, Henry RJ (2018) Evidence of inter-sectional chloroplast capture in Corymbia among sections Torellianae and Maculatae. Australian Journal of Botany 66, 369–378.
Evidence of inter-sectional chloroplast capture in Corymbia among sections Torellianae and Maculatae.Crossref | GoogleScholarGoogle Scholar |

Hill K, Johnson L (1995) Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6, 185–504.
Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |

Jones ME, Shepherd M, Henry R, Delves A (2008) Pollen flow in Eucalyptus grandis determined by paternity analysis using microsatellite markers. Tree Genetics & Genomes 4, 37–47.
Pollen flow in Eucalyptus grandis determined by paternity analysis using microsatellite markers.Crossref | GoogleScholarGoogle Scholar |

Kikuchi R, Jae-Hong P, Takahashi H, Maki M (2010) Disjunct distribution of chloroplast DNA haplotypes in the understory perennial Veratrum album ssp. oxysepalum (Melanthiaceae) in Japan as a result of ancient introgression. New Phytologist 188, 879–891.
Disjunct distribution of chloroplast DNA haplotypes in the understory perennial Veratrum album ssp. oxysepalum (Melanthiaceae) in Japan as a result of ancient introgression.Crossref | GoogleScholarGoogle Scholar |

Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15, 1179–1191.
Clumpak: a program for identifying clustering modes and packaging population structure inferences across K.Crossref | GoogleScholarGoogle Scholar | 25684545PubMed |

Levy E, Byrne M, Coates DJ, Macdonald BM, McArthur S, van Leeuwen S (2016) Contrasting influences of geographic range and distribution of populations on patterns of genetic diversity in two sympatric Pilbara acacias. PLoS ONE 11, e0163995
Contrasting influences of geographic range and distribution of populations on patterns of genetic diversity in two sympatric Pilbara acacias.Crossref | GoogleScholarGoogle Scholar | 27768703PubMed |

Ley AC, Hardy OJ (2010) Species delimitation in the Central African herbs Haumania (Marantaceae) using georeferenced nuclear and chloroplastic DNA sequences. Molecular Phylogenetics and Evolution 57, 859–867.
Species delimitation in the Central African herbs Haumania (Marantaceae) using georeferenced nuclear and chloroplastic DNA sequences.Crossref | GoogleScholarGoogle Scholar | 20813193PubMed |

Librado P, Rozas J (2009) DnaSP v.5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
DnaSP v.5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 19346325PubMed |

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

Maddison WP, Maddison DR (2016) Mesquite: a modular system for evolutionary analysis. Available at http://mesquiteproject.org.

McKinnon GE, Jordan GJ, Vaillancourt RE, Steane DA, Potts BM (2004) 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, 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 | GoogleScholarGoogle Scholar | 20298471PubMed |

Mimura M, Barbour RC, Potts BM, Vaillancourt RE, Watanabe KN (2009) Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests. Molecular Ecology 18, 4180–4192.
Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests.Crossref | GoogleScholarGoogle Scholar | 19769693PubMed |

Muir G, Schlötterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Molecular Ecology 14, 549–561.
Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.).Crossref | GoogleScholarGoogle Scholar | 15660945PubMed |

Nicolle D (2019) Classification of the eucalypts (Angophora, Corymbia and Eucalyptus) Version 4. Available at http://www.dn.com.au/Classification-Of-The-Eucalypts.

Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology 13, 1143–1155.
Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants.Crossref | GoogleScholarGoogle Scholar | 15078452PubMed |

Ochieng JW, Shepherd M, Baverstock PR, Nikles G, Lee DJ, Henry RJ (2010) Two sympatric spotted gum species are molecularly homogeneous. Conservation Genetics 11, 45–56.
Two sympatric spotted gum species are molecularly homogeneous.Crossref | GoogleScholarGoogle Scholar |

Parra-O C, Bayly MJ, Drinnan A, Udovicic F, Ladiges P (2009) Phylogeny, major clades and infrageneric classification of Corymbia (Myrtaceae), based on nuclear ribosomal DNA and morphology. Australian Systematic Botany 22, 384–399.
Phylogeny, major clades and infrageneric classification of Corymbia (Myrtaceae), based on nuclear ribosomal DNA and morphology.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar | 22820204PubMed |

Pickett EJ (1997) ‘A Late Pleistocene and Holocene vegetation history of three lacustrine sequences from the Swan Coastal Plain.’ (The University of Western Australia: Perth, WA, Australia)

Pollock LJ, Bayly MJ, Nevill PG, Vesk PA (2013) Chloroplast DNA diversity associated with protected slopes and valleys for hybridizing Eucalyptus species on isolated ranges in south-eastern Australia. Journal of Biogeography 40, 155–167.
Chloroplast DNA diversity associated with protected slopes and valleys for hybridizing Eucalyptus species on isolated ranges in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237–1245.
Measuring and testing genetic differentiation with ordered versus unordered alleles.Crossref | GoogleScholarGoogle Scholar | 8913764PubMed |

Posada D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 18397919PubMed |

Prideaux GJ, Gully GA, Couzens AMC, Ayliffe LK, Jankowski NR, Jacobs Z, Roberts RG, Hellstrom JC, Gagan MK, Hatcher LM (2010) Timing and dynamics of Late Pleistocene mammal extinctions in southwestern Australia. Proceedings of the National Academy of Sciences of the United States of America 107, 22157–22162.
Timing and dynamics of Late Pleistocene mammal extinctions in southwestern Australia.Crossref | GoogleScholarGoogle Scholar | 21127262PubMed |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Inference of population structure using multilocus genotype data.Crossref | GoogleScholarGoogle Scholar | 10835412PubMed |

Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.
Statistical properties of new neutrality tests against population growth.Crossref | GoogleScholarGoogle Scholar | 12446801PubMed |

Robins TP, Binks RM, Byrne M, Hopper SD (2021) Landscape and taxon age are associated with differing patterns of hybridization in two Eucalyptus (Myrtaceae) subgenera. Annals of Botany 127, 49–62.
Landscape and taxon age are associated with differing patterns of hybridization in two Eucalyptus (Myrtaceae) subgenera.Crossref | GoogleScholarGoogle Scholar | 32914170PubMed |

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 |

Sampson JF, Byrne M (2008) Outcrossing between an agroforestry plantation and remnant native populations of Eucalyptus loxophleba. Molecular Ecology 17, 2769–2781.
Outcrossing between an agroforestry plantation and remnant native populations of Eucalyptus loxophleba.Crossref | GoogleScholarGoogle Scholar | 18444981PubMed |

Sampson JF, Hankinson M, Mcarthur S, Tapper S, Langley M, Gibson N, Yates C, Byrne M (2015) Long-term ‘islands’ in the landscape: low gene flow, effective population size and genetic divergence in the shrub Hakea oldfieldii (Proteaceae). Botanical Journal of the Linnean Society 179, 319–334.
Long-term ‘islands’ in the landscape: low gene flow, effective population size and genetic divergence in the shrub Hakea oldfieldii (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Sampson J, Tapper S, Coates D, Hankinson M, Mcarthur S, Byrne M (2018) Persistence with episodic range expansion from the early Pleistocene: the distribution of genetic variation in the forest tree Corymbia calophylla (Myrtaceae) in south-western Australia. Biological Journal of the Linnean Society. Linnean Society of London 123, 545–560.
Persistence with episodic range expansion from the early Pleistocene: the distribution of genetic variation in the forest tree Corymbia calophylla (Myrtaceae) in south-western Australia.Crossref | GoogleScholarGoogle Scholar |

Schaal BA, Leverich WJ (2001) Plant population biology and systematics. Taxon 50, 679–695.
Plant population biology and systematics.Crossref | GoogleScholarGoogle Scholar |

Shepherd M, Kasem S, Ablett G, Ochieng J, Crawford A (2008) Genetic structuring in the spotted gum complex (genus Corymbia, section Politaria). Australian Systematic Botany 21, 15–25.
Genetic structuring in the spotted gum complex (genus Corymbia, section Politaria).Crossref | GoogleScholarGoogle Scholar |

Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.Crossref | GoogleScholarGoogle Scholar | 2513255PubMed |

Tapper SL, Byrne M, Yates CJ, Keppel G, Hopper SD, Van Niel K, Schut AGT, Mucina L, Wardell-Johnson GW (2014) Isolated with persistence or dynamically connected? Genetic patterns in a common granite outcrop endemic. Diversity and Distributions 20, 987–1001.
Isolated with persistence or dynamically connected? Genetic patterns in a common granite outcrop endemic.Crossref | GoogleScholarGoogle Scholar |

Thornhill AH, Macphail M (2012) Fossil myrtaceous pollen as evidence for the evolutionary history of Myrtaceae: a review of fossil Myrtaceidites species. Review of Palaeobotany and Palynology 176–177, 1–23.
Fossil myrtaceous pollen as evidence for the evolutionary history of Myrtaceae: a review of fossil Myrtaceidites species.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |

Wang J (2017) The computer program structure for assigning individuals to populations: easy to use but easier to misuse. Molecular Ecology Resources 17, 981–990.
The computer program structure for assigning individuals to populations: easy to use but easier to misuse.Crossref | GoogleScholarGoogle Scholar | 28028941PubMed |

Wang J, Wu Y, Ren G, Guo Q, Liu J, Lascoux M (2011) Genetic differentiation and delimitation between ecologically diverged Populus euphratica and P. pruinosa. PLoS ONE 6, e26530
Genetic differentiation and delimitation between ecologically diverged Populus euphratica and P. pruinosa.Crossref | GoogleScholarGoogle Scholar | 22028897PubMed |

Whitlock BA, Hale AM, Groff PA (2010) Intraspecific inversions pose a challenge for the trnH–psbA plant DNA barcode. PLoS ONE 5, e11533
Intraspecific inversions pose a challenge for the trnH–psbA plant DNA barcode.Crossref | GoogleScholarGoogle Scholar | 20644717PubMed |