Abstract
Genetic variation in drought damage in Eucalyptus globulus was studied in a sublined trial series across four neighbouring sites in Western Australia linked by ten common families. The trials included approximately 400 open-pollinated families, encompassing 51 native stand collection localities and 19 subraces from throughout the geographic range of the species. Data were analysed using mixed models, with spatial analysis used to better identify genetic effects. Significant subrace differences in drought damage were detected, with both broad-scale, regional and localised clines evident. The quantitative genetic differentiation between subraces as measured by Q ST (0.39 ± 0.091) was significantly greater than the F ST for neutral marker expectations and consistent with diversifying selection shaping the patterns of subrace divergence in drought susceptibility. This conclusion is supported by the significant association of subrace drought susceptibility with bioclimatic parameters, particularly those associated with temperature seasonality. Less drought damage was observed in subraces originating from areas with more temperature seasonality, but also less radiation and rainfall seasonality, less winter rainfall, higher radiation and higher temperatures in the warmest month. Significant additive genetic variation in drought damage was detected within subraces, with narrow-sense heritabilities ranging from 0.14 to 0.20. We argue that spatial genetic variation in drought susceptibility of E. globulus has been shaped by natural selection acting at multiple scales and discuss opportunities for exploiting this genetic variation in breeding and deployment programs.
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Aitken SN, Yeaman S, Holliday JA, Wang TL, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684
Anderson JE, Williams J, Kriedemann PE, Austin MP, Farquhar GD (1996) Correlations between carbon isotope discrimination and climate of native habitats for diverse eucalypt taxa growing in a common garden. Aust J Plant Physiol 23:311–320
Anekonda TS, Lomas MC, Adams WT, Kavanagh KL, Aitken SN (2002) Genetic variation in drought hardiness of coastal Douglas-fir seedlings from British Columbia. Can J For Res 32:1701–1716
Astorga R, Soria F, Basurco F, Toval G (2004) Diversity analysis and genetic structure of Eucalyptus globulus Labill. In: Borralho NMG, Pereira JS, Marques C, Coutinho J, Madeira M, Tomé M (eds) Eucalyptus in a changing world. Proceedings of an IUFRO Conference. RAIZ, Aveiro, Portugal, pp 351–363
Australian Bureau of Meteorology (2010a) Australia’s Climate. Year Book of Australia, 2009–10. Australian Bureau of Statistics, Canberra
Australian Bureau of Meteorology (2010b) Climate Data Online. Bureau of Meterology, Daily and monthly rainfall records (Accessed 20 October 2010)
Battaglia M, Bruce J, Brack C, Baker T (2009) Climate change and Australia’s plantation estate: analysis of vulnerability and preliminary investigation of adaptation options. Forest & Wood Products Australia Limited Report. Forest & Wood Products Australia, Canberra, p 125
Berlin M, Danell Ö, Jansson G, Andersson B, Elfving B, Ericsson T (2009a) A model to estimate economic weight of tree survival relative to volume production taking patchiness into account. Scand J For Res 24:278–287
Berlin M, Jansson G, Danell Ö, Andersson B, Elfving B, Ericsson T (2009b) Economic weight of tree survival relative to volume production in tree breeding: a case study with Pinus sylvestris in northern Sweden. Scand J For Res 24:288–297
Broadmeadow MSJ, Ray D, Samuel CJA (2005) Climate change and the future for broadleaved tree species in Britain. Forestry 78:145–161
Brooksbank K, Crombie D, Butcher T (1997) Early identification of drought tolerance in Eucalyptus globulus families. In: Higa AR, Schaitza E, Gaiad S (eds) IUFRO conference on silviculture and improvement of eucalypts. EMBRAPA, Salvador, Bahia, Brazil, pp 125–131
Bureau of Rural Sciences (2010) Australia’s forests at a glance. Bureau of Rural Sciences, Canberra, p 96
Caldeira MD, Fernandez V, Tome J, Pereira JS (2002) Positive effect of drought on longicorn borer larval survival and growth on eucalyptus trunks. Ann For Sci 59:99–106
Calder JA, Kirkpatrick JB (2008) Climate change and other factors influencing the decline of the Tasmanian cider gum (Eucalyptus gunnii). Aust J Bot 56:684–692
Callister AN, Arndt SK, Ades PK, Merchant A, Rowell D, Adams MA (2008) Leaf osmotic potential of Eucalyptus hybrids responds differently to freezing and drought, with little clonal variation. Tree Physiol 28:1297–1304
Chambers PGS, Borralho NMG (1997) Importance of survival in short-rotation tree breeding programs. Can J For Res 27:911–917
Correia I, Almeida MH, Aguiar A, Alía R, David TS, Pereira JS (2008) Variations in growth, survival and carbon isotope composition (δ13C) among Pinus pinaster populations of different geographic origins. Tree Physiol 28:1545–1552
Costa e Silva J, Dutkowski GW, Gilmour AR (2001) Analysis of early tree height in forest genetic trials is enhanced by including a spatially correlated residual. Can J For Res 31:1887–1893
Costa e Silva J, Potts BM, Dutkowski G (2006) Genotype by environment interaction for growth of Eucalyptus globulus in Australia. Tree Genet Genome 2:61–75
Crisp M, Cook L, Steane D (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about evolution of diversity in present-day communities? Philos Trans R Soc Lond, Ser B: Biol Sci 359:1551–1571
Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679
Dutkowski GW (1995) Genetic variation in drought susceptibility of Eucalyptus globulus ssp. globulus in plantations in Western Australia. In: Potts BM, Borralho NMG, Reid JB, Cromer RN, Tibbits WN, Raymond CA (eds) Eucalypt plantations: improving fibre yield and quality. CRC for Temperate Hardwood Forestry, Hobart, Tasmania, pp 199–203
Dutkowski GW, Potts BM (1999) Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification. Aust J Bot 47:237–263
Dutkowski GW, Gilmour AR, Borralho NMG (2001) Modification of the additive relationship matrix for open pollinated trials. In: Developing the eucalypt of the future. INFOR, Valdivia, Chile
Dutkowski GW, Costa e Silva J, Gilmour AR, Lopez GA (2002) Spatial analysis methods for forest genetic trials. Can J For Res 32:2201–2214
Dutkowski GW, Costa e Silva J, Gilmour AR, Wellendorf H, Aguiar A (2006) Spatial analysis enhances modelling of a wide variety of traits in forest genetic trials. Can J For Res 36:1851–1870
Edelaar P, Björklund M (2011) If F ST does not measure neutral genetic differentiation, then comparing it with Q ST is misleading. Or is it? Mol Ecol 20:1805–1812
Eldridge K, Davidson J, Harwood C, van Wyk G (1993) Eucalypt domestication and breeding. Clarendon Press, Oxford, UK
Falconer DS (1989) Introduction to quantitative genetics. Wiley, New York
Foster SA, McKinnon GE, Steane DA, Potts BM, Vaillancourt RE (2007) Parallel evolution of dwarf ecotypes in the forest tree Eucalyptus globulus. New Phytol 175:370–380
Gailing O, Vornam B, Leinemann L, Finkeldey R (2009) Genetic and genomic approaches to assess adaptive genetic variation in plants: forest trees as a model. Physiol Plant 137:509–519
Gardiner CA, Crawford DF (1987) Seed collections of Eucalyptus globulus subsp. globulus for tree improvement purposes. CSIRO Division of Forest Research, Canberra
Gardiner CA, Crawford DF (1988) Seed collections of Eucalyptus globulus subsp. globulus Labill. for tree improvement purposes. CSIRO Division of Forestry and Forest Products, Canberra
Gavran M, Parsons M (2010) Australia’s plantations 2010 inventory update, national forest inventory. Bureau of Rural Sciences, Canberra, Australia, p 8
Gianola D, Norton HW (1981) Scaling threshold characters. Genetics 99:357–364
Gibson A, Hubick KT, Bachelard EP (1991) Effects of abscisic-acid on morphological and physiological-responses to water-stress in Eucalyptus camaldulensis seedlings. Aust J Plant Physiol 18:153–163
Gibson A, Bachelard EP, Hubick KT (1995) Relationship between climate and provenance variation in Eucalyptus camaldulensis Dehnh. Aust J Plant Physiol 22:453–460
Gilmour AR, Anderson RD, Rae AL (1987) Variance components on an underlying scale for ordered multiple threshold categorical data using a generalized linear mixed model. J Anim Breed Genet 104:149–155
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, UK
Guarnaschelli AB, Lemcoff JH, Prystupa P, Basci SO (2003) Responses to drought preconditioning in Eucalyptus globulus Labill. provenances. Trees 17:501–509
Guarnaschelli AB, Prystupa P, Lemcoff JH (2006) Drought conditioning improves water status, stomatal conductance and survival of Eucalyptus globulus subsp bicostata seedlings. Ann For Sci 63:941–950
Hamann A, Gylander T, Py C (2010) Developing seed zones and transfer guidelines with multivariate regression trees. Tree Genet Genome 7:399–408
Hamilton M, Tilyard P, Williams D, Vaillancourt R, Wardlaw T, Potts B (2011) The genetic variation in the timing of heteroblastic transition in Eucalyptus globulus is stable across environments. Aust J Bot 59:170–175
Hanks LM, Paine TD, Millar JG, Campbell CD, Schuch UK (1999) Water relations of host trees and resistance to the phloem-boring beetle Phoracantha semipunctata F. (Coleoptera: Cerambycidae). Oecologia 119:400–407
Harper RJ, Smettem KRJ, Carter JO, McGrath JF (2009) Drought deaths in Eucalyptus globulus (Labill.) plantations in relation to soils, geomorphology and climate. Plant Soil 324:199–207
Hellmann JJ, Pineda-Krch M (2007) Constraints and reinforcement on adaptation under climate change: selection of genetically correlated traits. Biol Conserv 137:599–609
Henderson CR (1984) Applications of linear models in animal breeding. University of Guelph, Guelph
Hodge GR, Volker PW, Potts BM, Owen JV (1996) A comparison of genetic information from open-pollinated and control-pollinated progeny tests in two eucalypt species. Theor Appl Genet 92:53–63
Houlder DJ, Hutchinson MF, Nix HA, McMahon JP (2000) ANUCLIM users guide, version 5.1. Australian National University, Canberra, Australia
Hughes L, Cawsey EM, Westoby M (1996) Climatic range sizes of Eucalyptus species in relation to future climate change. Glob Ecol Biogeogr Lett 5:23–29
Johansson S, Tuomela K (1996) Growth of 16 provenances of Eucalyptus microtheca in a regularly irrigated plantation in eastern Kenya. For Ecol Manag 82:11–18
Jones R (2009) Molecular evolution and genetic control of flowering in Eucalyptus globulus species complex. PhD Thesis, University of Tasmania
Jones TH, Steane DA, Jones RC, Pilbeam D, Vaillancourt RE, Potts BM (2006) Effects of domestication on genetic diversity in Eucalyptus globulus. For Ecol Manag 234:78–84
Jordan GJ, Potts BM, Kirkpatrick JB, Gardiner C (1993) Variation in the Eucalyptus globulus complex revisited. Aust J Bot 41:763–785
Jordan GJ, Potts BM, Chalmers P, Wiltshire RJE (2000) Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp globulus is an adaptive trait. Aust J Bot 48:561–567
Jump AS, Cavin L, Hunter PD (2010) Monitoring and managing responses to climate change at the retreating range edge of forest trees. J Environ Monit 12:1791–1798
Kramer AT, Havens K (2009) Plant conservation genetics in a changing world. Trends Plant Sci 14:599–607
Kremer A (2007) How well can existing forests withstand climate change? In: Koskela J, Buck A, Teisser du Cross E (eds) Climate change and forest genetic diversity: implications for sustainable management in Europe. Biodiversity International, Rome, Italy, pp 3–17
Kremer A, Le Corre V, Petit R, Ducousso A (2010) Historical and contemporary dynamics of adaptive differentiation in European oaks. In: DeWoody A, Bickham JW, Michler C, Nichols KM, Rhodes OE Jr, Woeste K (eds) Molecular approaches in natural resource conservation and management. Cambridge University, Cambridge, UK, pp 101–122
Kuparinen A, Savolainen O, Schurr FM (2010) Increased mortality can promote evolutionary adaptation of forest trees to climate change. For Ecol Manag 259:1003–1008
Ladiges PY (1974) Variation in drought tolerance in Eucalyptus viminalis Labill. Aust J Bot 22:489–500
Li CY (1998) Variation of seedling traits of Eucalyptus microtheca origins in different watering regimes. Silvae Genet 47:132–136
Li CY (1999) Carbon isotope composition, water-use efficiency and biomass productivity of Eucalyptus microtheca populations under different water supplies. Plant Soil 214:165–171
Li CY, Wang KY (2003) Differences in drought responses of three contrasting Eucalyptus microtheca F. Muell. populations. For Ecol Manag 179:377–385
Lopez GA, Potts BM, Dutkowski GW, Traverso JMR (2001) Quantitative genetics of Eucalyptus globulus: affinities of land race and native stand localities. Silvae Genet 50:244–252
López R, Rodríguez-Calcerrada J, Gil L (2009) Physiological and morphological response to water deficit in seedlings of five provenances of Pinus canariensis: potential to detect variation in drought-tolerance. Trees Struct Funct 23:509–519
Meier IC, Leuschner C (2008) Genotypic variation and phenotypic plasticity in the drought response of fine roots of European beech. Tree Physiol 28:297–309
Merchant A, Ladiges PY, Adams MA (2007) Quercitol links the physiology, taxonomy and evolution of 279 eucalypt species. Glob Ecol Biogeogr 16:810–819
Mokotedi MEO (2010) Physiological responses of Eucalyptus nitens × nitens under experimentally imposed water stress. South For 72:63–68
O’Brien EK, Mazanec RA, Krauss SL (2007) Provenance variation of ecologically important traits of forest trees: implications for restoration. J Appl Ecol 44:583–593
Ogren E, Evans JR (1992) Photoinhibition of photosynthesis in situ in 6 species of Eucalyptus. Aust J Plant Physiol 19:223–232
Osorio J, Pereira JS (1994) Genotypic differences in water use efficiency and C-13 discrimination in Eucalyptus globulus. Tree Physiol 14:871–882
Osorio J, Osorio ML, Chaves MM, Pereira JS (1998a) Effects of water deficits on C-13 discrimination and transpiration efficiency of Eucalyptus globulus clones. Aust J Plant Physiol 25:645–653
Osorio J, Osorio ML, Chaves MM, Pereira JS (1998b) Water deficits are more important in delaying growth than in changing patterns of carbon allocation in Eucalyptus globulus. Tree Physiol 18:363–373
Phillips OL, van der Heijden G, Lewis SL, López-González G, Aragão LEOC et al (2010) Drought-mortality relationships for tropical forests. New Phytol 187:631–646
Pita P, Pardos JA (2001) Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit. Tree Physiol 21:599–607
Pita P, Soria F, Cañas I, Toval G, Pardos JA (2001) Carbon isotope discrimination and its relationship to drought resistance under field conditions in genotypes of Eucalyptus globulus Labill. For Ecol Manag 141:211–221
Potts BM, Vaillancourt RE, Jordan GJ, Dutkowski GW, Costa e Silva J et al (2004) Exploration of the Eucalyptus globulus gene pool. In: Borralho NMG, Pereira JS, Marques C, Coutinho J, Madeira M, Tomé M (eds) Eucalyptus in a changing world. RAIZ Instituto Investigação de Floresta e Papel, Aveiro, Portugal, pp 46–61
Prado JA, Infante P, Ipinza R, Bañados JC (1991) Juvenile growth and drought resistance of 166 families of Eucalyptus camaldulensis in the semi-arid region of Chile. In: Schönau APG (ed) Intensive forestry: the role of eucalypts. Proceedings of an IUFRO symposium. Southern African Institute of Forestry, Durban, South Africa, pp 276–286
R Core Development Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
Ramírez-Valiente JA, Lorenzo Z, Soto A, Valladares F, Gil L, Aranda I (2009) Elucidating the role of genetic drift and natural selection in cork oak differentiation regarding drought tolerance. Mol Ecol 18:3803–3815
Ramírez-Valiente JA, Valladares F, Delgado Huertas A, Granados S, Aranda I (2010) Factors affecting cork oak growth under dry conditions: local adaptation and contrasting additive genetic variance within populations. Tree Genet Genome 7:285–295
Sánchez-Gómez D, Majada J, Alía R, Feito I, Aranda I (2010) Intraspecific variation in growth and allocation patterns in seedlings of Pinus pinaster Ait. submitted to contrasting watering regimes: can water availability explain regional variation? Ann For Sci 67(5):505
Savolainen O, Pyhajarvi T, Knurr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38:595–619
Schiller G, Korol L, Shklar G (2004) Habitat effects on adaptive genetic variation in Pinus halepensis Mill. provenances. For Genet 11:325–335
Sederoff R, Myburg A, Kirst M (2009) Genomics, domestication, and evolution of forest trees. Cold Spring Harbor Symp Quant Biol 74:303–317
Soria F, Borralho NMG (1998) The genetics of resistance to Phoracantha semipunctata attack in Eucalyptus globulus in Spain. Silvae Genet 46:365–369
St Clair JB, Howe GT (2007) Genetic maladaptation of coastal Douglas-fir seedlings to future climates. Glob Chang Biol 13:1441–1454
Stackpole DJ, Vaillancourt RE, Downes GM, Harwood CE, Potts BM (2010) Genetic control of kraft pulp yield in Eucalyptus globulus. Can J For Res 40:917–927
Stackpole D, Vaillancourt R, Alves A, Rodrigues J, Potts B (2011) Genetic variation in the chemical components of Eucalyptus globulus wood. G3: Genes, Genomes Genetics 1:151–159
Steane DA, Conod N, Jones RC, Vaillancourt RE, Potts BM (2006) A comparative analysis of population structure of a forest tree, Eucalyptus globulus (Myrtaceae), using microsatellite markers and quantitative traits. Tree Genet Genome 2:30–38
Sthultz CM, Gehring CA, Whitham TG (2009) Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species. Glob Chang Biol 15:1949–1961
Stram DO, Lee JW (1994) Variance components testing in the longitudinal mixed effects model. Biometrics 50:1171–1177
Susiluoto S, Berninger F (2007) Interactions between morphological and physiological drought responses in Eucalyptus microtheca. Silva Fenn 41:221–233
Tausz M, Merchant A, Kruse J, Samsa G, Adams MA (2008) Estimation of drought-related limitations to mid-rotation aged plantation grown Eucalyptus globulus by phloem sap analysis. For Ecol Manag 256:844–848
Teulières C, Bossinger G, Moran G, Marque C (2007) Stress studies in Eucalyptus. Plant Stress 1:197–215
Toro MA, Silió L, Rodriguez MC, Soria F, Toval G (1998) Genetic analysis of survival to drought in Eucalyptus globulus in Spain. 6th World Congress on Genetics Applied to Livestock Production, Armidale, Australia, pp 499-502
Toval G (2004) The Eucalyptus globulus clonal silviculture in Mediterranean climate. In: Borralho NMG, Pereira JS, Marques C, Coutinho J, Madeira M, Tomé M (eds) Eucalyptus in a changing world. RAIZ, Instituto Investigação de Floresta e Papel, Aveiro, Portugal, pp 70–78
White DA, Beadle CL, Worledge D (2000) Control of transpiration in an irrigated Eucalyptus globulus Labill. plantation. Plant Cell Environ 23:123–134
White TL, Adams WT, Neale DB (2007) Forest genetics. CABI, Wallingford UK
White D, Battaglia M, Bruce J, Benyon R, Beadle C et al (2009a) Water-use efficient plantations–separating the wood from the leaves. Forest & Wood Products Australia Limited Report. Forest & Wood Products Australia, Canberra, Australia, p 25
White DA, Crombie DS, Kinal J, Battaglia M, McGrath JF, Mendham DS, Walker SN (2009b) Managing productivity and drought risk in Eucalyptus globulus plantations in south-western Australia. For Ecol Manag 259:33–44
Whitehead D, Beadle CL (2004) Physiological regulation of productivity and water use in Eucalyptus: a review. For Ecol Manag 193:113–140
Whitlock MC (2008) Evolutionary inference from Qst. Mol Ecol 17:1885–1896
Whittock SP, Apiolaza LA, Kelly CM, Potts BM (2003) Genetic control of coppice and lignotuber development in Eucalyptus globulus. Aust J Bot 51:57–67
Ye TZ, Jayawickrama KJS (2008) Efficiency of using spatial analysis in first-generation coastal Douglas-fir progeny tests in the US Pacific Northwest. Tree Genet Genome 4:677–692
Acknowledgements
The authors acknowledge the contribution of Bunnings Treefarms (now WA Plantation Resources-WAPRES) and the former Western Australian Tree Breeding Association (particularly Trevor Butcher) for establishing and maintaining the trials used in this analysis and for the permission of WAPRES to collect, analyse and publish the data. Furthermore, we would like to thank Mark Hovenden for running ANUCLIM for us, the various staff members of the School of Plant Science who willingly looked at our many graphs to help with the interpretation, Don White and René Vaillancourt for their contribution to helpful discussions and Don White and Tony McRae for comments on the manuscript. Funding for this study was provided by an Australian Research Council Linkage Grant (LP0884001) which has the Southern Tree Breeding Association, seedEnergy Pty Ltd and PlantPlan Genetics Pty Ltd as partner organisations.
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Dutkowski, G.W., Potts, B.M. Genetic variation in the susceptibility of Eucalyptus globulus to drought damage. Tree Genetics & Genomes 8, 757–773 (2012). https://doi.org/10.1007/s11295-011-0461-8
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DOI: https://doi.org/10.1007/s11295-011-0461-8