A phylogenetic investigation of the taxonomically problematic Eucalyptus odorata complex (E. section Adnataria series Subbuxeales): evidence for extensive interspecific gene flow and reticulate evolution
Patrick S. Fahey
A B * , Frank Udovicic D , David J Cantrill D , Dean Nicolle E , Todd G. B. McLay C E and Michael J. Bayly C
+ Author Affiliations
- Author Affiliations
A Queensland Alliance of Agriculture and Food Innovation, University of Queensland, St Lucia, Qld, Australia.
B Research Centre for Ecosystem Resilience, Australian Institute of Botanical Science, The Royal Botanic Garden, Sydney, NSW, Australia.
C Currency Creek Arboretum, Melrose Park, SA, Australia.
D School of BioSciences, The University of Melbourne, Parkville, Vic., Australia.
E National Herbarium of Victoria, Royal Botanic Gardens Victoria, South Yarra, Vic., Australia.
Australian Systematic Botany 35(5) 403-435 https://doi.org/10.1071/SB21029
Submitted: 30 July 2021 Accepted: 20 September 2022 Published: 20 October 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
To investigate the relationships among species in the taxonomically problematic Eucalyptus odorata species complex, we generated molecular data using double-digest restriction site-associated DNA sequencing (ddRADseq) and Diversity Arrays Technology sequencing (DArTseq). These data were analysed utilising principal-component analysis (PCA), phylogenetic networks, phylogeny reconstruction and hybridisation tests. Twelve species that are variously recognised in the complex were sampled from across their ranges, along with co-occurring members of E. section Adnataria, to allow for patterns of hybridisation and gene flow to be identified. Despite the large genetic datasets generated, many relationships within the E. odorata complex were poorly resolved, and few species were monophyletic, likely owing to both biological factors including recent speciation and extensive hybridisation and introgression, and potential over-splitting of taxa. We show that multiple taxa with limited distributions are the result of reticulate evolutionary events and that typical Eucalyptus viridis R.T.Baker and the possibly con-specific E. aenea K.D.Hill are sister to the rest of the complex. The remaining species appeared to represent a discontinuous crescent-shaped cline running from the Flinders Ranges to the south-western slopes region of New South Wales, with limited support for an east–west split in this cline across the Murray River Basin. Eucalytpus viridis var. latiuscula Blakely, which is not closely related to the typical variety of this species in our data, may represent a northern extension to this cline.
Keywords: biogeography, DArTseq, ddRADseq, Eucalyptus, hybridisation, phylogenetics, reticulate evolution, south-eastern Australia.
References
Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D (2013) Hybridization and speciation. Journal of Evolutionary Biology 26, 229–246.| Hybridization and speciation.Crossref | GoogleScholarGoogle Scholar |
Aguirre NC, Filippi CV, Zaina G, Rivas JG, Acuña CV, Villalba PV, García MN, González S, Rivarola M, Martínez MC, Puebla AF, Morgante M, Hopp HE, Paniego NB, Marcucci Poltri SN (2019) Optimizing ddRADseq in non-model species: a case study in Eucalyptus dunnii Maiden. Agronomy 9, 484
| Optimizing ddRADseq in non-model species: a case study in Eucalyptus dunnii Maiden.Crossref | GoogleScholarGoogle Scholar |
Alwadani KG, Janes JK, Andrew RL (2019) Chloroplast genome analysis of box-ironbark Eucalyptus. Molecular Phylogenetics and Evolution 136, 76–86.
| Chloroplast genome analysis of box-ironbark Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160, 1217–1229.
| A model-based method for identifying species hybrids using multilocus genetic data.Crossref | GoogleScholarGoogle Scholar |
Baum D (1992) Phylogenetic species concepts. Trends in Ecology & Evolution 7, 1–2.
| Phylogenetic species concepts.Crossref | GoogleScholarGoogle Scholar |
Bean AR (2009) Taxonomic and nomenclatural notes on the Eastern grey boxes (Eucalyptus ser. Moluccanae Chippendale, Myrtaceae) and the reinstatement of Eucalyptus woollsiana R.T.Baker. Austrobaileya 8, 25–34.
Blakely WF (1934) ‘A key to the eucalypts: with descriptions of 500 species and 138 varieties, and a companion to J. H. Maiden’s critical revision of the genus Eucalyptus.’ (The Worker Trustees: Sydney, NSW, Australia)
Bradburd GS, Coop GM, Ralph PL (2018) Inferring continuous and discrete population genetic structure across space. Genetics 210, 33–52.
| Inferring continuous and discrete population genetic structure across space.Crossref | GoogleScholarGoogle Scholar |
Brooker MIH (2000) A new classification of the genus Eucalyptus L’Hér. (Myrtaceae). Australian Systematic Botany 13, 79–148.
| A new classification of the genus Eucalyptus L’Hér. (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Brooker MIH, Nicolle D (2013) ‘Atlas of leaf venation and oil gland patterns in the eucalypts.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Brooker MIH, Slee AV, Connors JR, Duffy S, West J (2015) ‘EUCLID: eucalypts of Australia’, 4th edn. (CSIRO: Canberra, ACT, Australia)
Chippendale GM (1988) ‘Flora of Australia. Vol. 19: Myrtaceae – Eucalyptus, Angophora.’ (Australian Government Publishing Service: Canberra, ACT, Australia)
Collins RA, Hrbek T (2015) An in silico comparison of reduced-representation and sequence-capture protocols for phylogenomics. bioRxiv 2015, 032565
| An in silico comparison of reduced-representation and sequence-capture protocols for phylogenomics.Crossref | GoogleScholarGoogle Scholar |
Copeland LM, Hunter JT (2005) Range extension, habitat and conservation status of three rare mallees, Eucalyptus castrensis, Eucalyptus fracta and Eucalyptus pumila from the Hunter Valley, NSW. Cunninghamia 9, 307–309.
Council of Heads of Australasian Herbaria (2016) ‘Australian Plant Census, IBIS database. Centre for Australian National Biodiversity Research.’ (Australian Government: Canberra, ACT, Australia)
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27, 2156–2158.
| The variant call format and VCFtools.Crossref | GoogleScholarGoogle Scholar |
Durand EY, Patterson N, Reich D, Slatkin M (2011) Testing for ancient admixture between closely related populations. Molecular Biology And Evolution 28, 2239–2252.
| Testing for ancient admixture between closely related populations.Crossref | GoogleScholarGoogle Scholar |
Eaton DAR, Overcast I (2020) ipyrad: interactive assembly and analysis of RADseq datasets. Bioinformatics 36, 2592–2594.
| ipyrad: interactive assembly and analysis of RADseq datasets.Crossref | GoogleScholarGoogle Scholar |
Fahey PS, Fowler RM, McLay TGB, Udovicic F, Cantrill DJ, Bayly MJ (2021) Divergent lineages in a semi-arid mallee species, Eucalyptus behriana, correspond to a major geographic break in southeastern Australia. Ecology and Evolution 11, 664–678.
| Divergent lineages in a semi-arid mallee species, Eucalyptus behriana, correspond to a major geographic break in southeastern Australia.Crossref | GoogleScholarGoogle Scholar |
Flores-Rentería L, Rymer PD, Riegler M (2017) Unpacking boxes: integration of molecular, morphological and ecological approaches reveals extensive patterns of reticulate evolution in box eucalypts. Molecular Phylogenetics and Evolution 108, 70–87.
| Unpacking boxes: integration of molecular, morphological and ecological approaches reveals extensive patterns of reticulate evolution in box eucalypts.Crossref | GoogleScholarGoogle Scholar |
Griffin AR, Burgess IP, Wolf L (1988) Patterns of natural and manipulated hybridisation in the genus Eucalyptus L’Hérit. – 1. A review. Australian Journal of Botany 36, 41–66.
| Patterns of natural and manipulated hybridisation in the genus Eucalyptus L’Hérit. – 1. A review.Crossref | GoogleScholarGoogle Scholar |
Gruber B, Unmack PJ, Berry OF, Georges A (2018) dartR: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources 18, 691–699.
| dartR: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing.Crossref | GoogleScholarGoogle Scholar |
Guo C, Ma P-F, Yang G-Q, Ye X-Y, Guo Y, Liu J-X, Liu Y-L, Eaton DAR, Guo Z-H, Li D-Z (2020) Parallel ddRAD and genome skimming analyses reveal a radiative and reticulate evolutionary history of the temperate bamboos. Systematic Biology 70, 756–773.
| Parallel ddRAD and genome skimming analyses reveal a radiative and reticulate evolutionary history of the temperate bamboos.Crossref | GoogleScholarGoogle Scholar |
Hill KD (1997) New species in Angophora and Eucalyptus (Myrtaceae) from New South Wales. Telopea 7, 97–109.
| New species in Angophora and Eucalyptus (Myrtaceae) from New South Wales.Crossref | GoogleScholarGoogle Scholar |
Hill KD, Stanberg LC (2002) Eucalyptus castrensis (Myrtaceae), a new species from New South Wales. Telopea 9, 773–776.
| Eucalyptus castrensis (Myrtaceae), a new species from New South Wales.Crossref | GoogleScholarGoogle Scholar |
Hines B, Byrne M (2001) Genetic differentiation between mallee and tree forms in the Eucalyptus loxophleba complex. Heredity 87, 566–572.
| Genetic differentiation between mallee and tree forms in the Eucalyptus loxophleba complex.Crossref | GoogleScholarGoogle Scholar |
Holman JE, Hughes JM, Fensham RJ (2003) A morphological cline in Eucalyptus: a genetic perspective. Molecular Ecology 12, 3013–3025.
| A morphological cline in Eucalyptus: a genetic perspective.Crossref | GoogleScholarGoogle Scholar |
Holman JE, Hughes JM, Fensham RJ (2011) Origins of a morphological cline between Eucalyptus melanophloia and Eucalyptus whitei. Australian Journal of Botany 59, 244–252.
| Origins of a morphological cline between Eucalyptus melanophloia and Eucalyptus whitei.Crossref | GoogleScholarGoogle Scholar |
Hopper S, Wardell-Johnson G (2004) Eucalyptus virginea and E. relicta (Myrtaceae), two new rare forest trees from south-western Australia allied to E. lanepoolei, and a new phantom hybrid. Nuytsia 15, 71–84.
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology And Evolution 23, 254–267.
| Application of phylogenetic networks in evolutionary studies.Crossref | GoogleScholarGoogle Scholar |
Jackson HD, Steane DA, Potts BM, Vaillancourt RE (1999) Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae). Molecular Ecology 8, 739–751.
| Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071.
| adegenet 1.3-1: new tools for the analysis of genome-wide SNP data.Crossref | GoogleScholarGoogle Scholar |
Jones RC, Nicolle D, Steane DA, Vaillancourt RE, Potts BM (2016) High density, genome-wide markers and intra-specific replication yield an unprecedented phylogenetic reconstruction of a globally significant, speciose lineage of Eucalyptus. Molecular Phylogenetics and Evolution 105, 63–85.
| High density, genome-wide markers and intra-specific replication yield an unprecedented phylogenetic reconstruction of a globally significant, speciose lineage of Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Jordan R, Hoffmann AA, Dillon SK, Prober SM (2017) Evidence of genomic adaptation to climate in Eucalyptus microcarpa: implications for adaptive potential to projected climate change. Molecular Ecology 26, 6002–6020.
| Evidence of genomic adaptation to climate in Eucalyptus microcarpa: implications for adaptive potential to projected climate change.Crossref | GoogleScholarGoogle Scholar |
Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In ‘Data production and analysis in population genomics. Vol. 888’. (Eds Pompanon F, Bonin A) pp. 67–89. (Humana Press: Totowa, NJ, USA)
Kirkpatrick JB, Simmons D, Parsons RF (1973) The relationship of some populations involving Eucalyptus cypellocarpa and E. globulus to the problem of phantom hybrids. New Phytologist 72, 867–876.
| The relationship of some populations involving Eucalyptus cypellocarpa and E. globulus to the problem of phantom hybrids.Crossref | GoogleScholarGoogle Scholar |
Kirschner P, Arthofer W, Pfeifenberger S, Záveská E, Schönswetter P, Steiner FM, Schlick-Steiner BC, The STEPPE Consortium (2021) Performance comparison of two reduced-representation based genome-wide marker-discovery strategies in a multi-taxon phylogeographic framework. Scientific Reports 11, 3978
| Performance comparison of two reduced-representation based genome-wide marker-discovery strategies in a multi-taxon phylogeographic framework.Crossref | GoogleScholarGoogle Scholar |
Knaus BJ, Grünwald NJ (2017) vcfr: a package to manipulate and visualize variant call format data in R. Molecular Ecology Resources 17, 44–53.
| vcfr: a package to manipulate and visualize variant call format data in R.Crossref | GoogleScholarGoogle Scholar |
Larcombe MJ, Holland B, Steane DA, Jones RC, Nicolle D, Vaillancourt RE, Potts BM (2015) Patterns of reproductive isolation in Eucalyptus: a phylogenetic perspective. Molecular Biology And Evolution 32, 1833–1846.
| Patterns of reproductive isolation in Eucalyptus: a phylogenetic perspective.Crossref | GoogleScholarGoogle Scholar |
Luo A, Ling C, Ho SYW, Zhu C-D (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology 67, 830–846.
| Comparison of methods for molecular species delimitation across a range of speciation scenarios.Crossref | GoogleScholarGoogle Scholar |
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10
| Cutadapt removes adapter sequences from high-throughput sequencing reads.Crossref | GoogleScholarGoogle Scholar |
Mayr E (1963) ‘Animal species and evolution.’ (Belknap Press of Harvard University Press: Cambridge, MA, USA)
Mayr E (2000) The biological species concept. In ‘Species concepts and phylogenetic theory: a debate’. (Eds QD Wheeler, R Meier) pp. 17–29. (Columbia University Press: New York, NY, USA)
McVean G (2009) A genealogical interpretation of principal components analysis. PLoS genetics 5, e1000686
| A genealogical interpretation of principal components analysis.Crossref | GoogleScholarGoogle Scholar |
Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan ARK, Hussey SG, Pinard D, van der Merwe K, Singh P, van Jaarsveld I, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye C-Y, Li T, Sterck L, Vanneste K, Murat F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Van de Peer Y, Rokhsar DS, Schmutz J (2014) The genome of Eucalyptus grandis. Nature 510, 356–362.
| The genome of Eucalyptus grandis.Crossref | GoogleScholarGoogle Scholar |
Nicolle D (2000) New taxa of Eucalyptus informal subgenus Symphyomyrtus (Myrtaceae), endemic to South Australia. Journal of the Adelaide Botanic Garden 19, 83–94.
Nicolle D (2006) ‘Eucalypts of Victoria and Tasmania.’ (Bloomings Books: Melbourne, Vic., Australia)
Nicolle D (2014) Myrtaceae (partly) (version 1). In ‘Flora of South Australia. Vol. 5’. (Ed. J Kellermann) (State Herbarium of South Australia: Adelaide, SA, Australia)
Nicolle D (2019) Classification of the eucalypts (Angophora, Corymbia and Eucalyptus) Version 4. Available at https://www.dn.com.au/Classification-Of-The-Eucalypts.pdf
Nicolle D, Roberts I (2013) ‘Native eucalypts of South Australia.’ (Dean Nicolle: Adelaide, SA, Australia)
O’Leary SJ, Puritz JB, Willis SC, Hollenbeck CM, Portnoy DS (2018) These aren’t the loci you’e looking for: principles of effective SNP filtering for molecular ecologists. Molecular Ecology 27, 3193–3206.
| These aren’t the loci you’e looking for: principles of effective SNP filtering for molecular ecologists.Crossref | GoogleScholarGoogle Scholar |
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and geotyping in model and non-model species. PLoS One 7, e37135
| Double digest RADseq: an inexpensive method for de novo SNP discovery and geotyping in model and non-model species.Crossref | GoogleScholarGoogle Scholar |
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 |
Pryor LD, Johnson LAS (1971) ‘A classification of the eucalypts.’ (The Australian National University: Canberra, ACT, Australia)
Rule K (1990) Eucalyptus wimmerensis, a new species of Eucalyptus (Myrtaceae) from Victoria and South Australia. Muelleria 7, 193–201.
| Eucalyptus wimmerensis, a new species of Eucalyptus (Myrtaceae) from Victoria and South Australia.Crossref | GoogleScholarGoogle Scholar |
Rule K (1994) Eucalyptus silvestris, a new species of Eucalyptus (Myrtaceae) for Victoria and South Australia and notes on Victorian occurrences of Eucalyptus odorata. Muelleria 8, 193–199.
| Eucalyptus silvestris, a new species of Eucalyptus (Myrtaceae) for Victoria and South Australia and notes on Victorian occurrences of Eucalyptus odorata.Crossref | GoogleScholarGoogle Scholar |
Rule K (2004) New taxa in Eucalyptus (Myrtaceae) for Victoria and notes on Victorian populations of Eucalyptus calycogona. Muelleria 20, 9–32.
| New taxa in Eucalyptus (Myrtaceae) for Victoria and notes on Victorian populations of Eucalyptus calycogona.Crossref | GoogleScholarGoogle Scholar |
Rule K (2012) Five new endemic eucalypts for Victoria. Muelleria 30, 83–105.
| Five new endemic eucalypts for Victoria.Crossref | GoogleScholarGoogle Scholar |
Rule K (2018) Eucalyptus wimmerensis revisited and notes on the morphologies and taxonomies of five Victorian mallee-boxes. Muelleria 37, 39–64.
| Eucalyptus wimmerensis revisited and notes on the morphologies and taxonomies of five Victorian mallee-boxes.Crossref | GoogleScholarGoogle Scholar |
Rutherford S, Wilson PG, Rossetto M, Bonser SP (2016) Phylogenomics of the green ash eucalypts (Myrtaceae): a tale of reticulate evolution and misidentification. Australian Systematic Botany 28, 326–354.
| Phylogenomics of the green ash eucalypts (Myrtaceae): a tale of reticulate evolution and misidentification.Crossref | GoogleScholarGoogle Scholar |
Rutherford S, Rossetto M, Bragg JG, McPherson H, Benson D, Bonser SP, Wilson PG (2018) Speciation in the presence of gene flow: population genomics of closely related and diverging Eucalyptus species. Heredity 121, 126–141.
| Speciation in the presence of gene flow: population genomics of closely related and diverging Eucalyptus species.Crossref | GoogleScholarGoogle Scholar |
Rutherford S, van der Merwe M, Wilson PG, Kooyman RM, Rossetto M (2019) Managing the risk of genetic swamping of a rare and restricted tree. Conservation Genetics 20, 1113–1131.
| Managing the risk of genetic swamping of a rare and restricted tree.Crossref | GoogleScholarGoogle Scholar |
Rutherford S, Wan JSH, Cohen JM, Benson D, Rossetto M (2020) Looks can be deceiving: speciation dynamics of co-distributed Angophora (Myrtaceae) species in a varying landscape. Evolution 75, 310–329.
| Looks can be deceiving: speciation dynamics of co-distributed Angophora (Myrtaceae) species in a varying landscape.Crossref | GoogleScholarGoogle Scholar |
Sansaloni CP, Petroli CD, Carling J, Hudson CJ, Steane DA, Myburg AA, Grattapaglia D, Vaillancourt RE, Kilian A (2010) A high-density diversity arrays technology (DArT) microarray for genome-wide genotyping in Eucalyptus. Plant Methods 6, 16
| A high-density diversity arrays technology (DArT) microarray for genome-wide genotyping in Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Schuster TM, Setaro SD, Tibbits JFG, Batty EL, Fowler RM, McLay TGB, Wilcox S, Ades PK, Bayly MJ (2018) Chloroplast variation is incongruent with classification of the Australian bloodwood eucalypts (genus Corymbia, family Myrtaceae). PLoS One 13, e0195034
| Chloroplast variation is incongruent with classification of the Australian bloodwood eucalypts (genus Corymbia, family Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Stamatakis A (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
| RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar |
Steane DA, Byrne M, Vaillancourt RE, Potts BM (1998) Chloroplast DNA polymorphism signals complex interspecific interactions in Eucalyptus (Myrtaceae). Australian Systematic Botany 11, 25–40.
| Chloroplast DNA polymorphism signals complex interspecific interactions in Eucalyptus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Steane DA, Nicolle D, McKinnon GE, Vaillancourt RE, Potts BM (2002) Higher-level relationships among the eucalypts are resolved by ITS-sequence data. Australian Systematic Botany 15, 49–62.
| Higher-level relationships among the eucalypts are resolved by ITS-sequence data.Crossref | GoogleScholarGoogle Scholar |
Steane DA, Nicolle D, Potts BM (2007) Phylogenetic positioning of anomalous eucalypts by using ITS sequence data. Australian Systematic Botany 20, 402–408.
| Phylogenetic positioning of anomalous eucalypts by using ITS sequence data.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Steane DA, Potts BM, McLean EH, Collins L, Holland BR, Prober SM, Stock WD, Vaillancourt RE, Byrne M (2017) Genomic scans across three eucalypts suggest that adaptation to aridity is a genome-wide phenomenon. Genome Biology and Evolution 9, 253–265.
| Genomic scans across three eucalypts suggest that adaptation to aridity is a genome-wide phenomenon.Crossref | GoogleScholarGoogle Scholar |
Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11, 7
| TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Swofford D (2002) ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0.’ (Sinauer Associates: Sunderland, MA, USA)
Thornhill AH, Crisp MD, Külheim C, Lam KE, Nelson LA, Yeates DK, Miller JT (2019) A dated molecular perspective of eucalypt taxonomy, evolution and diversification. Australian Systematic Botany 32, 29–48.
| A dated molecular perspective of eucalypt taxonomy, evolution and diversification.Crossref | GoogleScholarGoogle Scholar |
Wickham H (2016) ‘ggplot2: Elegant Graphics for Data Analysis.’ (Springer-Verlag: New York, NY, USA)
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 | GoogleScholarGoogle Scholar |
Yang G-Q, Chen Y-M, Wang J-P, Guo C, Zhao L, Wang X-Y, Guo Y, Li L, Li D-Z, Guo Z-H (2016) Development of a universal and simplified ddRAD library preparation approach for SNP discovery and genotyping in angiosperm plants. Plant Methods 12, 39
| Development of a universal and simplified ddRAD library preparation approach for SNP discovery and genotyping in angiosperm plants.Crossref | GoogleScholarGoogle Scholar |
Zheng Y, Janke A (2018) Gene flow analysis method, the D-statistic, is robust in a wide parameter space. BMC Bioinformatics 19, 10
| Gene flow analysis method, the D-statistic, is robust in a wide parameter space.Crossref | GoogleScholarGoogle Scholar |
