Genetic and morphological analysis of multi-stemmed plants of tuart (Eucalyptus gomphocephala)
M. Byrne A C , A. Koenders B C D , K. Rogerson A B , J. Sampson A and E. J. B. van Etten B
+ Author Affiliations
- Author Affiliations
A Science and Conservation Division, Department of Parks and Wildlife, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia.
B Centre for Ecosystem Management, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA 6027, Australia.
C Joint first authors.
D Corresponding author. Email: a.koenders@ecu.edu.au
Australian Journal of Botany 64(8) 704-714 https://doi.org/10.1071/BT16091
Submitted: 6 May 2016 Accepted: 1 November 2016 Published: 22 November 2016
Abstract
The tuart–banksia woodlands of the Swan Coastal Plain in Western Australia are characteristic vegetation communities of this coastal region, and Eucalyptus gomphocephala DC. (Myrtaceae; tuart) is an iconic tree of these communities. The species primarily occurs as a tall single-stemmed tree, but at the northern end of the distribution, it also occurs in a multi-stemmed form. Growth habit is frequently used as a taxonomic character in eucalypts, with many complexes having tree and mallee forms, although the genetic characterisation of growth habit in eucalypts has been limited. We investigated the genetic and morphological differentiation among populations of tree and multi-stemmed forms of tuart at the northern end of its distribution. Although the populations showed moderate levels of genetic diversity on the basis of microsatellite markers, as might be expected from populations on the periphery of the distribution, there was no evidence of genetic differentiation associated with the tree and multi-stemmed forms. Morphometric analysis showed some differences in the size of buds and fruits among the populations. Our analysis is consistent with environmentally induced variation in tuart in near-coastal populations where plants grow on poor soils and form may be affected by wind and salt exposure. This result adds to other evidence from pines and Nothofagus of environmental rather than genetic influences on growth form, particularly in stressful environments.
Additional keywords: growth habit, microsatellites, morphometric analysis, population genetics.
References
Archibald RD, Bradshaw J, Bowen BJ, Close DC, McCaw L, Drake PL, Hardy GESJ (2010) Understory thinning and burning trials are needed in conservation reserves: the case of tuart (Eucalyptus gomphocephala DC.). Ecological Management & Restoration 11, 108–112.| Understory thinning and burning trials are needed in conservation reserves: the case of tuart (Eucalyptus gomphocephala DC.).Crossref | GoogleScholarGoogle Scholar |
Barbour RC, Potts BM, Vaillancourt RE (2005) Pollen dispersal from exotic eucalypt plantations. Conservation Genetics 6, 253–257.
| Pollen dispersal from exotic eucalypt plantations.Crossref | GoogleScholarGoogle Scholar |
Barrera MD, Frangi JL, Ricther LL, Perdomo MH, Pinedo LB (2000) Structural and functional changes in Nothofagus pumilio forests along an altitudinal gradient in Tierra del Fuego, Argentina. Journal of Vegetation Science 11, 179–188.
| Structural and functional changes in Nothofagus pumilio forests along an altitudinal gradient in Tierra del Fuego, Argentina.Crossref | GoogleScholarGoogle Scholar |
Bradbury D, Krauss SL (2013) Limited impact of fragmentation and disturbance on the mating system of tuart (Eucalyptus gomphocephala, Myrtaceae): implications for seed-source quality in ecological restoration. Australian Journal of Botany 61, 148–160.
| Limited impact of fragmentation and disturbance on the mating system of tuart (Eucalyptus gomphocephala, Myrtaceae): implications for seed-source quality in ecological restoration.Crossref | GoogleScholarGoogle Scholar |
Brondani R, Brondani C, Tarchini R, Grattapaglia D (1998) Development, characterisation and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla. Theoretical and Applied Genetics 97, 816–827.
| Development, characterisation and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVaht7o%3D&md5=dc74fba61dad477084d5d564770e8168CAS |
Byrne M (2008a) 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)
Byrne M (2008b) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27, 2576–2585.
| Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography.Crossref | GoogleScholarGoogle Scholar |
Byrne M, Macdonald B, Francki M (2001) Incorporation of sodium sulphite into extraction protocol minimizes degradation of Acacia DNA. BioTechniques 30, 742–748.
Byrne M, Macdonald B, Brand J (2003) Phylogeography and divergence in the chloroplast genome of Western Australian sandalwood (Santalum spicatum). Heredity 91, 389–395.
| Phylogeography and divergence in the chloroplast genome of Western Australian sandalwood (Santalum spicatum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsF2msbY%3D&md5=6084bf92a8194c693bf0efd364398b40CAS |
Byrne M, Elliott C, Yates C, Coates D (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 |
Campagne P, Smouse PE, Varouchas G, Silvain JF, Leru B (2012) Comparing the van Oosterhout and Chybicki–Burczyk methods of estimating null allele frequencies for inbred populations. Molecular Ecology Resources 12, 975–982.
| Comparing the van Oosterhout and Chybicki–Burczyk methods of estimating null allele frequencies for inbred populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFWju73N&md5=f81deef46bc5261cd48167851e19f48dCAS |
Carsey KS, Tomback DF (1994) Growth form distribution and genetic relationships in tree clusters of Pinus flexilis, a bird-dispersed pine. Oecologia 98, 402–411.
| Growth form distribution and genetic relationships in tree clusters of Pinus flexilis, a bird-dispersed pine.Crossref | GoogleScholarGoogle Scholar |
Chapuis MP, 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 | 1:CAS:528:DC%2BD2sXjtleku7c%3D&md5=4afaae5db4f772e729bead5a14674eb2CAS |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKmsA%3D%3D&md5=2645dad229bed0e51e57d2dfd3c3e84aCAS |
Clarke KR, Gorley RN (2006) ‘PRIMER v6: user manual/tutorial.’ (PRIMER-E: Plymouth, UK)
Coates DJ, Keighery GJ, Broadhurst LM (2002) Genetic and morphological variation, and the mating system in tuart. In ‘Tuart (Eucalyptus gomphocephala) and tuart communities’. (Eds BJ Keighery, VM Longman) pp. 89–107. (Wildflower Society of Western Australia, Perth Branch: Perth)
Cook IO, Ladiges PY (1991) Morphological variation within Eucalyptus nitens s.lat. and recognition of a new species, E. denticulata. Australian Systematic Botany 4, 375–390.
| Morphological variation within Eucalyptus nitens s.lat. and recognition of a new species, E. denticulata.Crossref | GoogleScholarGoogle Scholar |
Department of Conservation and Land Management, Tuart Response Group, and Ecoscape (2003) ‘An atlas of tuart woodlands on the Swan Coastal Plain in Western Australia.’ (Department of Conservation and Land Management: Perth)
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3, 167–169.
| Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivVyitbw%3D&md5=f0b60e9691819252f2fd08110040c21aCAS |
Doyle JJ, Doyle JL (1990) Isolation of DNA from fresh tissue. Focus 12, 13–15.
Earl DA, von Holdt 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 |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFShsbc%3D&md5=6c793e8ed3dd775c63592cf0de046630CAS |
Edwards TA (2004) Environmental correlates and associations of tuart (Eucalyptus gomphocephala) decline. Unpublished MSc Thesis, Edith Cowan University, Perth.
Fajardo A (2016) Are trait-scaling relationships invariant across contrasting elevations in the widely distributed treeline species Nothofagus pumilio? American Journal of Botany 103, 821–829.
| Are trait-scaling relationships invariant across contrasting elevations in the widely distributed treeline species Nothofagus pumilio? Crossref | GoogleScholarGoogle Scholar |
Fajardo A, McIntire EJB (2010) Merged trees in second-growth, fire origin forests in Patagonia, Chile: positive spatial association patterns and their ecological implications. American Journal of Botany 97, 1424–1430.
| Merged trees in second-growth, fire origin forests in Patagonia, Chile: positive spatial association patterns and their ecological implications.Crossref | GoogleScholarGoogle Scholar |
Fajardo A, Torres-Diaz C, Till-Bottraud I (2016) Disturbance and density-dependent processes (competition and facilitation) influence the fine-scale genetic structure of a tree species’ population. Annals of Botany 117, 67–77.
| Disturbance and density-dependent processes (competition and facilitation) influence the fine-scale genetic structure of a tree species’ population.Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (1989) phylip: phylogeny inference package (version 3.2). Cladistics 5, 164–166.
Grant MC, Mitton JB (1977) Genetic differentiation among growth forms of Englemann spruce and subalpine fir at tree line. Arctic and Alpine Research 9, 259–263.
| Genetic differentiation among growth forms of Englemann spruce and subalpine fir at tree line.Crossref | GoogleScholarGoogle Scholar |
Hill K, Johnson L (1992) Systematic studies in the eucalypts. 5. New taxa and combinations in Eucalyptus (Myrtaceae) in Western Australia. Telopea 4, 561–634.
| Systematic studies in the eucalypts. 5. New taxa and combinations in Eucalyptus (Myrtaceae) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Hines B, Byrne M (2001) Genetic differentiation of mallee and tree forms in the Eucalyptus loxophleba complex. Heredity 87, 566–572.
| Genetic differentiation of mallee and tree forms in the Eucalyptus loxophleba complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFWntrk%3D&md5=6f55146e367978f207ddc420803f2197CAS |
Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 1322–1332.
| Inferring weak population structure with the assistance of sample group information.Crossref | GoogleScholarGoogle Scholar |
Ishaq L, Barber PA, Hardy GESJ, Calver M, Dell B (2013) Seedling mycorrhizal type and soil chemistry are related to canopy condition of Eucalyptus gomphocephala. Mycorrhiza 23, 359–371.
| Seedling mycorrhizal type and soil chemistry are related to canopy condition of Eucalyptus gomphocephala.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsVyrtb8%3D&md5=d4937af94d46ad4ffca84a86d4511840CAS |
Jacobs MR (1955) ‘Growth habits of the eucalypts.’ (Forestry and Timber Bureau: Canberra)
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1ahtbs%3D&md5=1ea408b69fff497fc7bfdaecd713d04bCAS |
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 | 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 |
Jost L (2008) G ST and its relatives do not measure differentiation. Molecular Ecology 17, 4015–4026.
| G ST and its relatives do not measure differentiation.Crossref | GoogleScholarGoogle Scholar |
Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Molecular Ecology Notes 5, 187–189.
| HP-Rare: a computer program for performing rarefaction on measures of allelic diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFyms7k%3D&md5=02c46154bc4e28ddc8f23232d627134fCAS |
Keighery BJ, Keighery GJ, Shepherd D (2002) The distribution and conservation of tuart and the community with which it lives. In ‘Tuart (Eucalyptus gomphocephala) and tuart communities’. (Eds BJ Keighery, VM Longman) pp. 6–74. (Wildflower Society of Western Australia, Perth Branch: Perth)
Lacey CJ, Johnson RD (1990) Woody clumps and clumpwoods. Australian Journal of Botany 38, 299–334.
| Woody clumps and clumpwoods.Crossref | GoogleScholarGoogle Scholar |
Ladiges PY (1997) Phylogenetic history and classification of eucalypts. In ‘Eucalypt ecology: individuals to ecosystems’. (Eds JE Williams, JCZ Woinarski) pp. 16- 29. (Cambridge University Press: Cambridge, UK)
Linhart YB, Tomback DF (1985) Seed dispersal by nutcrackers causes multi-trunk growth form in pines. Oecologia 67, 107–110.
| Seed dispersal by nutcrackers causes multi-trunk growth form in pines.Crossref | GoogleScholarGoogle Scholar |
Longman V, Keighery B (2002) Tuart issues. In ‘Tuart (Eucalyptus gomphocephala) and tuart communities’. (Eds BJ Keighery, VM Longman) pp. 292–330. (Wildflower Society of Western Australia, Perth Branch: Perth)
Maiden JH (1924) ‘A critical revision of the genus Eucalyptus.’ (William Applegate Gullick: Sydney)
Main AR (1996) Ghosts of the past: where does environmental history begin? Environment and History 2, 97–114.
| Ghosts of the past: where does environmental history begin?Crossref | GoogleScholarGoogle Scholar |
Martin HA (1989) Evolution of mallee and its environment. In ‘Mediterranean landscapes in Australia, mallee ecosystems and their management’. (Eds JC Noble JC, RA Bradstock) pp. 83–92. (CSIRO Publications: Melbourne)
McIntire EJB, Fajardo A (2011) Facilitation within species: a possible origin of group-selected superorganisms. American Naturalist 178, 88–97.
| Facilitation within species: a possible origin of group-selected superorganisms.Crossref | GoogleScholarGoogle Scholar |
Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Molecular Ecology Resources 11, 5–18.
| Assessing population structure: F ST and related measures.Crossref | GoogleScholarGoogle Scholar |
Nevill PG, Bradbury D, Williams A, Tomlinson S, Krauss SL (2014) Genetic and palaeo-climatic evidence for widespread persistence of the coastal tree species Eucalyptus gomphocephala (Myrtaceae) during the Last Glacial Maximum. Annals of Botany 113, 55–67.
| Genetic and palaeo-climatic evidence for widespread persistence of the coastal tree species Eucalyptus gomphocephala (Myrtaceae) during the Last Glacial Maximum.Crossref | GoogleScholarGoogle Scholar |
Nicolle D (2006) A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus – Myrtaceae) with special reference to obligate seeders. Australian Journal of Botany 54, 391–407.
| A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus – Myrtaceae) with special reference to obligate seeders.Crossref | GoogleScholarGoogle Scholar |
Nicolle D, Byrne M, Whalen M (2005) A taxonomic revision and morphological variation within Eucalyptus series Subulatae subseries Oleaginae (Myrtaceae) including the oil mallee complex, of south-western Australia. Australian Systematic Botany 18, 525–553.
| A taxonomic revision and morphological variation within Eucalyptus series Subulatae subseries Oleaginae (Myrtaceae) including the oil mallee complex, of south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Nistelberger N, Gibson N, Macdonald B, Tapper S-L, Byrne M (2014) Phylogeographic evidence for two mesic refugia in a biodiversity hotspot. Heredity 113, 454–463.
| Phylogeographic evidence for two mesic refugia in a biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWisLbE&md5=240ae229973d6057eaf8a03081c4ef09CAS |
Ottewell KM, Donnellan SC, Lowe AJ, Paton DC (2009) Predicting reproductive success of insect- versus bird-pollinated scattered trees in agricultural landscapes. Biological Conservation 142, 888–898.
| Predicting reproductive success of insect- versus bird-pollinated scattered trees in agricultural landscapes.Crossref | GoogleScholarGoogle Scholar |
Passioura JA, Ash JE (1993) Phenotypic, genetic and ecological variation in the Eucalyptus saligna–E. botryoides complex. Australian Journal of Botany 41, 393–412.
| Phenotypic, genetic and ecological variation in the Eucalyptus saligna–E. botryoides complex.Crossref | GoogleScholarGoogle Scholar |
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 |
Peakall R, Smouse PE (2012) genelex 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update. Bioinformatics 28, 2537–2539.
| genelex 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=3aedf299f887f0505d198a30f656894dCAS |
Phillips RL, Reid JB (1980) Clinal variation between Eucalyptus viminalis Labill. and E. dalrympleana Maiden. Australian Journal of Botany 28, 329–342.
| Clinal variation between Eucalyptus viminalis Labill. and E. dalrympleana Maiden.Crossref | GoogleScholarGoogle Scholar |
Powell R (1990) ‘Leaf and branch: trees and tall shrubs of Perth.’ (Department of Conservation and Land Management: Perth)
Powell R, Keighery BJ (2002). Tuart in the landscape. In ‘Tuart (Eucalyptus gomphocephala) and tuart communities’. (Eds VM Longman, BJ Keighery) pp. 279–286. (Perth Branch Wildflower Society of Western Australia (Inc.): Perth)
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155, 945–959.
Pryor LD (1957) The inheritance of some characters in Eucalyptus. Proceedings of the Linnean Society of New South Wales 82, 199–200.
Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecology and Evolution 4, 4399–4428.
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1SltbY%3D&md5=b239fbda0b6ca467b9b969b40ba4da61CAS |
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 |
Ruthroff KX, Yates CJ, Lonergan CJ (2002) The biology of tuart. In ‘Tuart (Eucalyptus gomphocephala) and tuart communities’. (Eds BJ Keighery, VM Longman) pp. 89–107. (Wildflower Society of Western Australia, Perth Branch: Perth)
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 |
Shea KL, Grant MC (1986) Clonal growth in spire-shaped Englemann spruce and subalpine fir trees. Canadian Journal of Botany 64, 255–261.
| Clonal growth in spire-shaped Englemann spruce and subalpine fir trees.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.
Till-Bottraud I, Fajardo A, Rioux D (2012) Multi-stemmed trees of Nothofagus pumilio second-growth forest in Patagonia are formed by highly related individuals. Annals of Botany 110, 905–913.
| Multi-stemmed trees of Nothofagus pumilio second-growth forest in Patagonia are formed by highly related individuals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yhu7%2FF&md5=4e425be51efa023ac02ae9b57cbacfbaCAS |
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 | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=3e3a229671f1af2cf8cc2a9369847b8eCAS |
