Abstract
Eucalyptus camaldulensis is one of the most widely utilised eucalypts. It is also the only eucalypt that occurs across the Australian continent, playing a key ecological role as fauna habitat and in riverbank stabilisation. Despite its ecological and economic importance, uncertainty remains regarding the delineation of genetic and morphological variants. Nine hundred and ninety trees from 97 populations, representing the species’ geographic range were genotyped using 15 microsatellite loci and patterns of diversity compared with restriction fragment length polymorphisms in 29 of these populations. Both markers showed that despite having a riverine distribution, downstream seed dispersal has had less influence than geographic distance on dispersal patterns. Spatial patterns in the distribution of microsatellite genotypes were compared with environmental parameters and boundaries defined by river systems, drainage basins and proposed subspecies. Significant genetic differences among populations within river systems indicated that rivers should not be treated as a single genetic entity in conservation or breeding programmes. Strong geographic trends were evident with 40% of variation in genetic diversity explained by latitude and moisture index. Isolation by distance and significant correlations between genetic distance and environmental parameters for most loci suggest historical factors have had more influence than selection on current patterns of distribution of genetic diversity. Geographic structuring of molecular variation, together with congruence between genetic and morphological variation indicate that E. camaldulensis should be treated as a number of subspecies rather than a single variable taxon. High levels of genetic diversity and geographic trends in the distribution of variation provide a firm basis for further exploration of the species’ genetic resources.
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References
Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190
AUSLIG (2001) Australian Surveying and Land Information Group, Australian Drainage Divisions and River Basin Boundaries. Available on the Australian Bureau of Meteorology website, http://www.bom.gov.au/hydro/wr/basins. Accessed 17 Dec 2007
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2008) GenBank. Nucleic Acids Res 36(Database Issue):D25–D30
Birtchnell MJ, Gibson M (2006) Long-term flowering patterns in melliferous Eucalyptus (Myrtaceae) species. Aust J Bot 54:745–754
Blake ST (1953) Botanical contributions of the Northern Australia Regional Survey. I. Studies on northern Australian species of Eucalyptus. Aust J Bot 1:268
Blakely WF (1935) A key to the eucalypts. Commonwealth Government Printer, Canberra
Blakers M, Davies SJJF, Reilly PN (1984) The atlas of Australian birds. Melbourne University Press, Melbourne
Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM, Johnston RD, Kleinig DA, McDonald MW, Turner JD (2006) Forest trees of Australia, 5th edn. CSIRO, Collingwood, pp 318–321
Brondani RPV, Brondani C, Tarchini R, Grattapaglia D (1998) Development, characterisation and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla. Theor Appl Genet 97:816–827
Brooker MIH (2000) A new classification of the genus Eucalyptus L’Hér. (Myrtaceae). Aust Syst Bot 13:79–148
Brooker MIH, Kleinig DA (2004) Field guide to eucalypts, Northern Australia, vol. 3. Bloomings Books, Melbourne
Butcher PA, Southerton S (2007) Marker-assisted selection in forestry species. In: Guimarães EP, Ruane J, Scherf BD, Sonnino A, Dargie JD (eds) Marker-assisted selection in crops, livestock, forestry and fish: current status and the way forward. FAO, Rome, pp 283–306
Butcher PA, Williams ER (2001) Variation in outcrossing rates and growth in Eucalyptus camaldulensis from the Petford Region Queensland; evidence of outbreeding depression. Silvae Genet 51:6–12
Butcher PA, Otero A, McDonald MW, Moran GF (2002) Nuclear RFLP variation in Eucalyptus camaldulensis Dehnh. from northern Australia. Heredity 88:402–412
Byrne M, Marquez-Garcia MI, Uren T, Smith DS, Moran GF (1996) Conservation and genetic diversity of microsatellite loci in the genus Eucalyptus. Aust J Bot 44:331–341
Cavalli-Sforza LL (1966) Population structure and human evolution. Proc Roy Soc Lond B 164:362–379
Clemson A (1985) Honey and pollen flora. Inkata, Melbourne
Cracraft J (1991) Patterns of diversification within continental biotas: hierarchical congruence among the areas of endemism of Australian vertebrates. Aust Syst Bot 4:211–227
Crisp MD, Cook L, Steane D (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Phil Trans Roy Soc Lond B 359:1551–1571
Davison A, Chiba S (2003) Laboratory temperature variation is a previously unrecognised source of genotyping error during capillary electrophoresis. Mol Ecol Notes 3:321–323
Dexter BD, Rose HJ, Davies N (1986) River regulation and associate forest management problems in the River Murray red gum forests. Aust For 49:16–27
Doran JC, Burgess IP (1993) Variation in floral bud morphology in the intergrading zones of Eucalyptus camaldulensis and E. tereticornis in Northern Queensland. Comm For Rev 72:198–202
Eldridge K, Davidson J, Harwood C, Wyk G (1993) Eucalypt domestication and breeding. Clarendon, Oxford, pp 60–71
Estoup A, Cornuet J-M (1999) Microsatellite evolution: inferences from population data. In: Goldstein DB, Schlötterer C (eds) Microsatellites: evolution and applications. Oxford University Press, Oxford, pp 49–65
Felsenstein J (1982) How can we infer geography and history from gene frequencies? J Theor Biol 96:9–20
Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) Version 3.67 http://evolution.gs.washington.edu/phylip.html. Accessed 20 Dec 2007
Frakes LA (1999) Evolution of Australian environments. In: Orchard AE, Thompson HS (eds) Flora of Australia, vol. 1 Introduction. Flora of Australia Series. CSIRO/Australian Biological Resources Study, Collingwood/Canberra
Gell GA, Bickford S (1996) Vegetation. In: Davies M, Twidale CR, Tyler MJ (eds) Natural history of the Flinders Ranges. Royal Society of South Australia/Department of Environment and Natural Resources, Adelaide, pp 86–101
Glaubitz JC (2004) convert: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310
Glaubitz JC, Emebiri LC, Moran GF (2001) Dinucleotide microsatellites from Eucalyptus sieberi: inheritance, diversity and improved scoring of single-base pair differences. Genome 44:1041–1045
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Accessed 20 Dec 2007
Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Mgt 197:323–335
Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evol 53:313–318
Hill RS (2004) Origins of the south–eastern Australian vegetation. Phil Trans Roy Soc Lond B 359:1537–1549
Hope GS (1994) Quaternary vegetation. In: Hill RS (ed) History of the Australian vegetation: Cretaceous to recent. Cambridge University Press, Cambridge, pp 368–389
Hopper SD, Harvey MS, Chappill JA, Main AR, Main BY (1996) The Western Australian biota as a Gondwanan heritage—a review. In: Hopper SD, Chappill JA, Harvey MS, George A (eds) Gondwanan heritage: past present and future of the West Australian biota. Surrey Beatty & Sons, Chipping Norton, pp 1–46
Houlder D, Hutchinson M, Nix HA, McMahon JP (2000) ANUCLIM, version 5.1. Centre for Resources and Environmental Studies, Australian National University, Canberra
Humphries CJ, Ladiges PY, Roos M, Zandee M (1991) Cladistic biogeography. In: Myers AA, Giller PS (eds) Analytical biogeography. Chapman and Hall, London, pp 337–404
Johnson C (2006) Australia’s mammal extinctions: a 50,000 year history. Cambridge University Press, New York
Jones T, Vaillencourt RE, Potts BM (2007) Detection and visualisation of spatial genetic structure in a continuous forest of Eucalyptus globulus. Mol Ecol 16:697–707
Kingsford RT (2000) Review: ecological impacts of dams, water diversions and river management on floodplain wetlands in Australia. Austral Ecol 25:109–127
Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data. Version 1.0 (d16c). http://lewis.eeb.uconn.edu/lewishome/software.html. Accessed 20 Dec 2007
Li Y-C, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465
Mabbutt JA (1969) Landforms of arid Australia. In: Slatyer RO, Perry RA (eds) Arid lands of Australia. Australian National University Press, Canberra, pp 11–32
Maiden JH (1920) A critical revision of the genus Eucalyptus, vol. IV. Government Printer, Sydney, pp 78–79
Maguire TL, Peakall R, Saenger P (2002) Comparative analysis of genetic diversity in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae) detected by AFLP and SSRs. Theor Appl Genet 104:388–389
Marcar N, Crawford DF (2004) Trees for saline landscapes. Publication no. 03/108. Rural Industries and Research Development Corporation, Canberra, pp 96–98
Mensforth LJ, Thorburn PJ, Tyerman SD, Walker GR (1994) Sources of water used by riparian Eucalyptus camaldulensis overlying highly saline groundwater. Oecologia 100:21–28
Midgley SJ, Eldridge KG, Doran JC (1989) Genetic resources of Eucalyptus camaldulensis Dehnh. Comm For Rev 68:295–308
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Nix HA (1982) Environmental determinants of biogeography and evolution in Terra Australis. In: Barker WR, Greenslade PJM (eds) Evolution of the flora and fauna of arid Australia. Peacock Publications, Frewville, pp 47–66
Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evol 57:1182–1195
Pettit NE, Froend RH (2001) Availability of seed for recruitment of riparian vegetation: a comparison of a tropical and temperate river system in Australia. Aust J Bot 49:515–528
Pryor LD (1953) Genetic control in Eucalyptus distribution. Proc Linn Soc NSW 78:8–18
Pryor LD, Johnson LAS (1971) A classification of the eucalypts. Australian National University, Canberra
Randell BR, Symon DE (1977) Distribution of Cassia and Solanum species in arid regions of Australia. Search 8:206–207
Raymond M, Rousset F (1995a) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249
Raymond M, Rousset F (1995b) An exact test for population differentiation. Evol 49:1280–1283
Schlötterer C, Wiehe T (1999) Microsatellites, a neutral marker to infer selective sweeps. In: Goldstein DB, Schlötterer C (eds) Microsatellites: evolution and applications. Oxford University Press, Oxford, pp 238–247
Silverton J, Servaes C, Biss P, Macleod D (2005) Reinforcement of reproductive isolation between adjacent populations in the Park Grass Experiment. Heredity 95:198–205
Singh G, Kershaw AP, Clark R (1980) Quaternary vegetation and fire history in Australia. In: Gill AM, Groves RH, Noble IR (eds) Fire and the Australian biota. Australian Academy of Sciences, Canberra, pp 23–54
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792
Slee AV, Brooker MIH, Duffy S, West J (2006) EUCLID—eucalypts of Australia. CD ROM. CSIRO, Melbourne
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573
Southerton SG, Birt P, Porter J, Ford HA (2004) Review of gene movement by bats and birds and its potential significance for eucalypt plantation forestry. Aust For 67:44–53
Steane DA, Vaillancourt RE, Russell J, Powell W, Marshall D, Potts BM (2001) Development and characterisation of microsatellite loci in Eucalyptus globulus (Myrtaceae). Silvae Genet 50:89–91
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thamarus KA, Groom K, Murrell J, Byrne M, Moran GF (2002) A genetic linkage map for Eucalyptus globulus with candidate loci for wood, fibre, and floral traits. Theor Appl Genet 104:379–387
Turnbull JW (1973) The ecology and variation of Eucalyptus camaldulensis Dehnh. FAO For Genet Res Inform 2:32–42
Twidale CR (2007) Ancient Australian landscapes. Rosenberg, Dural, pp 63–71
Weir BS (1996) Genetic data analysis II methods for discrete population genetic data. Sinauer, Sunderland
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol 38:1358–1370
White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in tropical dry forest: an example from Swietenia humilis. Proc Nat Acad Sci USA 99:2038–2042
Wyrwoll KH, McKenzie NL, Pederson BJ, Tapley IJ (1986) The great sandy desert of Northwestern Australia: the last 7000 years. Search 17:208–210
Acknowledgements
Many thanks to Andrew Slee, John Connors (CSIRO Plant Industry), Craig Gardiner, Glen Kile, John Larmour, Paul Macdonell, Stephen Midgley, Jock Morse, Tim Vercoe, Sarah Whitfeld (CSIRO Forest Biosciences, Australian Tree Seed Centre), Ian Brooker and Dean Nicolle for collection of leaf samples and field data, Guiseppina Morosin for technical assistance and Henry Nix for useful discussions concerning biogeography. We thank Ian Brooker, Suzanne Prober, Washington Gapare and two anonymous reviewers for useful comments on drafts of the manuscript. This research was funded by CSIRO.
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Butcher, P.A., McDonald, M.W. & Bell, J.C. Congruence between environmental parameters, morphology and genetic structure in Australia’s most widely distributed eucalypt, Eucalyptus camaldulensis . Tree Genetics & Genomes 5, 189–210 (2009). https://doi.org/10.1007/s11295-008-0169-6
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DOI: https://doi.org/10.1007/s11295-008-0169-6