Impact of fertility variation on genetic diversity and phenotypic traits in second generation seed production areas and clonal seed orchards of Eucalyptus camaldulensis

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Fertility and gene diversity were estimated in three second generation (F2) seed stands (SPA 1-3) and two clone trials (CSO 1&2) of Eucalyptus camaldulensis to assess the impact on seed crop. F2 seedlots were evaluated in comparison to native provenances, ten commercial clones and interspecific hybrids at diverse sites. SPA 1&2 were genetic gain trials of five first generation (F1) orchard seedlots, SPA 3 a plantation of one F1 orchard seedlot, and CSOs were clone trials of 21 commercial clones established at two contrasting sites. Fertility variation, as indicated by sibling coefficient, was high (Ψ, 9-14) in the SPAs as only about 26 % trees were fertile compared to 81 % trees in CSOs. Effective population size was higher in SPA 1 and 2 (Ns, 95 and 74, respectively) than SPA 3 (Ns = 39). Fertility was highly skewed in CSO 2 resulting in low effective population size (Ns = 2) compared to CSO 1 (Ns = 11). Constant seed collection enabled 3-fold increase in relative population size and 22 % higher predicted gene diversity in CSO 2. Genetic diversity (He) estimated using SSR markers was higher in SPA 1&2 and native provenances (NAT), compared to SPA 3 and CSO 1, whereas CSO 2 and clones had lower values. There was a high positive correlation between estimated He and predicted gene diversity values of SPAs and CSOs. He was positively correlated to mean field survival and negatively correlated to kraft pulp yield (KPY), evaluated at three years in progeny trials across three locations. Number of alleles per locus was higher in SPAs and native provenances compared to CSOs and clones. Discriminant principal component analysis clustered CSO, NAT and SPA seedlots in different groups while commercial E. camaldulensis clones clustered close to NAT. Multilocus outcrossing rate was generally high (tm, 91-100 %), though selfing was observed in two families of SPA 3 and CSO 2. Selected interspecific hybrid families of commercial E. camaldulensis clones (with E. urophylla and E. pellita) evaluated at two of the sites had higher He and KPY than clones at three years.

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  • Arndt S Sanders G Hirsch M (2014) Hydraulic and ecophysiological traits related to tree drought mortality are linked to the aridity of the environment in eucalypts. Int Forest Rev 16(5): 236

  • Bezemer N Krauss SL Phillips RD Roberts DG Hopper SD (2016) Paternity analysis reveals wide pollen dispersal and high multiple paternity in a small isolated population of the bird-pollinated Eucalyptus caesia (Myrtaceae). Heredity (2016) 117 460–471.

  • Bila AD Lindgren D Mullin TJ (1999) Fertility variation and its effect on diversity over generations in a teak plantation (Tectona grandis L.f) Silvae Genet 48:109-114.

  • Bouvet JM Vigneron P Saya A (2005) Phenotypic plasticity of growth trajectory and ontogenic allometry in response to density for Eucalyptus hybrid clones and families. Ann Bot 96: 811–821.

  • Bouvet JM Saya A Vigneron P (2009) Trends in additive dominance and environmental effects with age for growth traits in Eucalyptus hybrid populations Euphytica 165 : 35-54.

  • Breed MF Christmas MJ Lowe AJ (2014) Higher levels of multiple paternities increase seedling survival in the long-lived tree Eucalyptus gracilis. PLoS ONE 9(2):1-9.

  • Burgess IP Williams ER Bell JC Harwood CE Owen JV (1996) The effect of outcrossing rate on the growth of selected families of Eucalyptus grandis. Silvae Genet 45 (2-3):97-100

  • Butcher PA Williams ER (2002) Variation in outcrossing rates and growth in Eucalyptus camaldulensis from the Petford Region Queensland; evidence of outbreeding depression. Silvae Genet 51:6–12

  • Chezhian P Yasodha R Modhumita Ghosh (2010) Genetic diversity analysis in a seed orchard of Eucalyptus tereticornis. New For. 40: 85–99.

  • Chaix G Gerber S Razafimaharo V Vigneron P Verhaegen D Hamon S (2003) Gene flow estimation with microsatellites in a Malagasy seed orchard of Eucalyptus grandis. Theor Appl Genet 107:705–712.

  • Chaix G Vigneron P Razafimaharo V Hamon S (2007) Are phenological observations sufficient to estimate the quality of seed crops from a Eucalyptus grandis open-pollinated seed orchard? consequences for seed collections. New For 33: 41-52.

  • Chaix G Vigneron P Razafimaharo V Hamon S (2010) Improved management of Malagasy Eucalyptus grandis seed orchards using microsatellites and paternity assessment. J Trop For Sci 22(3): 271–280.

  • Cornelius JP Clement CR Weber JC Sotelo-Montes C van Leeuwen J Ugarte-Guerra LJ Ricse-Tembladera A Arevalo-Lopez L (2006). The trade-off between genetic gain and conservation in a participatory improvement programme: the case of peach palm (Bactris gasipaes Kunth). Forests Trees and Livelihoods 2006 Vol. 16 pp. 17–34.

  • Danusevicius D Lindgren D (2010) Efficiency of breeding strategy where grandparents - but not parents - contribute equally to the breeding population. Ann. For. Sci. 67 (2010) 404.

  • Davidson J (1998) Domestication and breeding programme for Eucalyptus in the Asia-Pacific region. UNDP/FAO Regional Project on Improved Productivity of Man-Made Forests through Application of Technological Advances in Tree Breeding and Propagation (FORTIP) Philippines. 252p.

  • Dehon G Resende S Resende M Assis T (2013) A roadmap to eucalyptus breeding for clonal forestry. In: Fenning TM (ed) Challenges and opportunities for the world’s forests in the 21st century. Springer Dordrecht pp 394–424.

  • Doran JC Pinyopusarerk K Arnold R Harwood CE (1996) Breeding Plan for Eucalyptus camaldulensis in Tamil nadu. UNDP/FAO Regional Project on Improved Productivity of Man Made Forests through Application of Technical Advances in Tree Breeding and Propagation (RAS/91/004 – FORTIP) FAO Los Banos Phillipines 40p.

  • El-Kassaby YA (1992). Domestication and genetic diversity - should we be concerned? Forest Chron 68(6): 687-700.

  • El-Kassaby YA (1995) Evaluation of tree-improvement delivery system: factors affecting genetic potential. Tree Physiol 15:545-550.

  • Funda T El-Kassaby YA (2012) Seed orchard genetics. CAB Reviews 7(13): 1-23.

  • Funda T Lstibůrek M Lachout P Klápště J El-Kassaby YA (2009) Optimization of combined genetic gain and diversity for collection and deployment of seed orchard crops. Tree Genet Genomes 5: 583–593.

  • Gaiotto FA Bramucci M Grattapaglia D (1997) Estimation of out-crossing rate in a breeding population of Eucalyptus urophylla with dominant RAPD and AFLP markers. Theor Appl Genet 95:842–849.

  • Gardner RAW Little KM Arbuthnot A (2007) Wood and fibre productivity potential of promising new eucalypt species for coastal Zululand South Africa. Aust Forestry 70: 35-47.

  • Gonzaga JMS Manoel RO Sousa ACB Sousa AP Moraes MLT Freitas MLM Sebbenn AM (2016) Pollen contamination and non-random mating in a Eucalyptus camaldulensis Dehnh seedling seed orchard Silvae Genet 65(1): 1-11.

  • Griffin AR (2014) Clones or improved seedlings of Eucalyptus? Not a simple choice. Int Forest Rev 16:216–224.

  • Hardner C Dieters M DeLacy I Neal J Fletcher S Dale G Basford K (2011) Identifying deployment zones for Eucalyptus camaldulensis × E. globulus and × E. grandis hybrids using factor analytic modelling of genotype by environment interaction. Aust Forestry 74(1):30-35.

  • Harwood CE Nikles DG Pomroy PC Robson KW (1997) Genetic improvement of E. pellita in North Queensland Australia. In: Proceedings of the IUFRO Conference on Silviculture and improvement of eucalypt Salvador pp 219–226.

  • Hendre PS Kamalakannan R Varghese M (2012) High-throughput and parallel SNP discovery in selected candidate genes in Eucalyptus camaldulensis using Illumina NGS platform. Plant Biotech J 10:646-656.

  • Hou YC Yan ZH Wei YM Zheng YL (2005) Genetic diversity in barley from west China based on RAPD and ISSR analysis. Barley Genetics Newsletter 35:9–22

  • Hung TD Brawner JT Meder R Lee DJ Southerton S Thinh HH Dieters MJ (2015) Estimates of genetic parameters for growth and wood properties in Eucalyptus pellita F. Muell. to support tree breeding in Vietnam. Ann For Sci 72:205–217.

  • House APN Bell JC (1996) Genetic diversity mating system and systematic relationships in two red mahoganies Eucalyptus pellita and E. scias. Aust J Bot 44(2):157-174.

  • Ingvarsson PK Dahlberg H (2018) The effects of clonal forestry on genetic diversity in wild and domesticated stands of forest trees Scand J For Res

  • Ivetić V Devetaković J Nonić M Stanković D Šijačić-Nikolić M (2016) Genetic diversity and forest reproductive material - from seed source selection to planting. iForest 9:801-812.

  • Johnson R St. Clair B Lipow S (2001) Genetic conservation in applied tree breeding programs. In: Bart A Thielges BA Sastrapradja SD Rimbawanto A (eds) Proceedings of the ITTO Conference on In Situ and Ex Situ Conservation of Commercial Tropical Trees pp. 215–230. ITTO Yokohama Japan.

  • Jombart T (2008) adegenet: an R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405.

  • Jones TH Steane DA Jones RC Pilbeam D Vaillancourt RE Potts BM (2006) Effects of domestication on genetic diversity in Eucalyptus globulus. Forest Ecol Manag 234(1-3): 78-84.

  • Jones ME Shepherd M Henry R Delves A (2008) Pollen flow in Eucalyptus grandis determined by paternity analysis using microsatellite markers. Tree Genet Genomes (2008) 4:37–47.

  • Kalinowski ST Taper ML Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099-1106.

  • Kamalakannan R Suraj PG Arutselvan T Varghese M (2011) Early growth performance and wood properties of Eucalyptus interspecific hybrids at coastal and inland sites in southern India. In: IUFRO Conference on improvement and Culture of Eucalyptus Porto Seguro Brazil. Proceedings (ed.) Goncalves JLdeM Stape JL Grattapaglia D Voigtlaender M. Piracicaba: ESALQ 2011. 461-463p.

  • Kamalakannan R Varghese M Suraj PG Arutselvan T (2016) Options for converting a clone trial of Eucalyptus camaldulensis into a clonal seed orchard considering gain fertility and effective clone number. J For Res 27(1):51-57.

  • Kamalakannan R Varghese M Lindgren D (2007) Fertility variation and its implications on relatedness in seed crops in seedling seed orchards of Eucalyptus camaldulensis and E. tereticornis. Silvae Genet 56:253–259.

  • Kamalakannan R Varghese M Chezhian P Ghosh M Lindgren D (2009) Fertility variation and gene diversity in seed crops of Eucalyptus and Casuarina seedling seed orchards in southern India. In: Proceedings Seed Orchards Conference Jeju 8-11 September 2009. p 35.

  • Kang KS Lindgren D Mullin TJ (2001) Prediction of genetic gain and gene diversity in seed orchards crops under alternative management strategies. Theor Appl Genet 103(6–7):1099–1107.

  • Kang KS Bila AD Harju AM Lindgren D (2003). Estimation of fertility variation in forest tree populations. Forestry 76(3):329-344.

  • Kang KS Lindgren D (1999) Fertility variation among clones of Korean pine and its implications on seed orchard management. For Genet 6:191-200.

  • Krishnakumar N Sivakumar V Anandalakshmi R (2014) Eucalypt improvement in southern India. In: Bhojvaid PP Kaushik S Singh YP Kumar D Thapliyal M Barthwal S (eds) Eucalypts in India. Forest Research Institute Dehra Dun pp 139–148.

  • Kulkarni HD (2014) Eucalypt Improvement at ITC. In: Bhojvaid PP Kaushik S Singh YP Kumar D Thapliyal M Barthwal S (eds) Eucalypts in India. Forest Research Institute Dehra Dun pp 149–184.

  • Larcombe MJ Vaillancourt RE Jones RC Potts BM (2014) Assessing a bayesian approach for detecting exotic hybrids between plantation and native eucalypts International Journal of Forestry Research vol. 2014 Article ID 650202 13 pages 2014.

  • Lefevre F (2004) Human impacts on forest genetic resources in the temperate zone: An updated review. For Ecol Manag197: 257–271.

  • Leite SMM Mori ES do Valle CF Bonine CAV Marino CL (2008) RAPD analysis of genetic variability in a multiprovenance base population of Eucalyptus grandis Hill ex Maiden. R. Árvore Viçosa-MG 32(6): 961-967.

  • Leksono B Kurinobu S Ide Y (2008) Realised genetic gains observed in second generation seedling seed orchards of Eucalyptus pellita in Indonesia. J For Res 13:110–116.

  • Li Y Suontama M Burdon RD Dungey HS (2017) Genotype by environment interactions in forest tree breeding: review of methodology and perspectives on research and application. Tree Genet Genomes13: 60 – 77.

  • Libby WJ McCutchan BG Millar CI (1981) Inbreeding depression in selfs of redwood. Silvae Genet 30:15–25.

  • Lindgren D (2003) Low-input tree breeding strategies. In: Wei RP Xu D (eds) Eucalyptus plantations–research management and development. World Scientific Singapore pp 149–166

  • Lindgren D Mullin TJ (1998) Relatedness and status number in seed orchard crops. Can. J. For. Res. 28: 276–283.

  • Lindgren D Gea L Jefferson P (1996) Loss of genetic diversity monitored by status number. Silvae Genet 45:52-59.

  • Lu W Arnold RJ Zhang L Luo J (2018) Genetic diversity and structure through three cycles of a Eucalyptus urophylla S.T.Blake breeding program. Forests 9: 372-392.

  • Luo JZ Arnold RJ Cao JG Lu WH Ren SQ Xie YJ Xu LA (2012) Variation in pulp wood traits between eucalypt clones across sites and implications for deployment strategies. J Trop For Sci 24(1): 70–82.

  • Lyngdoh N Joshi G Ravikanth G Vasudeva R Uma Shaanker R (2013) Changes in genetic diversity parameters in unimproved and improved populations of teak (Tectona grandis L.f.) in Karnataka state India. J Genet 92(1):141-145.

  • Mora F Saavedra J (2012) Combining genetic gain and diversity under an individual selection method in a selected provenance of Eucalyptus cladocalyx. Plant Breeding Genetic and Genetic Resources Cien. Inv. Agr. 39(1):177-184.

  • Nagabhushana K Prasad SH Rajkumar R (2017) Intra and intergeneric transferable gene-derived orthologous microsatellite markers in Eucalyptus and Corymbia species. J For Res 22 (1) 65-68.

  • Na SJ Lee HS Han SU Park JM Kang KS (2015) Estimation of genetic gain and diversity under various genetic thinning scenarios in a breeding seed orchard of Quercus acutissima. Scand J For Res. 30: 377–38.

  • Nicodemus A Varghese M Nagarajan B Lindgren D (2009) Annual fertility variation in clonal seed orchards of teak (Tectona grandis L.f.) and its impact on seed crop. Silvae Genet 58: 85-93.

  • Park JM Kwon SH Lee HJ Na SJ El-Kassaby YAKang KS (2017) Integrating fecundity variation and genetic relatedness in estimating the gene diversity of seed crops: Pinus koraiensis seed orchard as an example. Can J For Res 47:366–370.

  • 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.

  • Pegg RE Wang GX (1994) Results of Eucalyptus pellita trials at Dongmen China. In: Brown A.G. (ed.) Australian tree species research in China: Proceedings of and international workshop held at Zhangzhou Fujian Province PRC 2-5 November ACIAR Proceedings No. 48. ACIAR Canberra pp.108–115.

  • Poltry SNM Zelener M Traverso JR Gelid P Hopp HE (2003) Selection of a seed orchard of Eucalyptus dunnii based on genetic diversity criteria calculated using molecular markers. Tree Physiol 23: 625-632.

  • Porth I El-Kassaby YA (2014) Assessment of the genetic diversity in forest tree populations using molecular markers. Diversity 2014 (6): 283-295.

  • Rao VR Hodgkin T (2002) Genetic diversity and conservation and utilization of plant genetic resources. Plant Cell Tiss Org 68: 1–19.

  • Resende RT Soares AAV Forrester DI Marcatti GE dos Santos AR Takahashi EK Silva FF Grattapaglia D Resende MDV Leite HG (2018) Environmental uniformity site quality and tree competition interact to determine stand productivity of clonal Eucalyptus. Forest Ecol Manag 410: 76-83.

  • Retief ECL Stanger TK (2009) Genetic parameters of pure and hybrid populations of Eucalyptus grandis and E. urophylla and implications for hybrid breeding strategy South For 71(2): 133 - 140.

  • Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88 (4):221-228.

  • Silva PHM Brune A Pupin S Moraes MLT Sebbenn AM de Paula RC (2018) Maintenance of genetic diversity in Eucalyptus urophylla S. T. Blake populations with restriction of the number of trees per family. Silvae Genet 67:34 – 40.

  • Sumathi M Yasodha R (2014) Microsatellite resources of Eucalyptus: current status and future perspectives. Bot Stud 55:73-88.

  • Tambarussi EV Boshier D Vencovsky R Menezes Freitas ML Sebbenn AM (2017) Inbreeding depression from selfing and mating between relatives in the Neotropical tree Cariniana legalis Mart. Kuntze. Conservation Genetics 18(1): 225-234.

  • Varghese M Nicodemus A Nagarajan B Subramanian K (2000) Hybrid breakdown in Mysore gum and need for genetic improvement of Eucalyptus camaldulensis and E. tereticornis. In: Hybrid Breeding and Genetics of Forest Trees Proceedings QFRI/CRC-SPF Symposium 9-14 April 2000 Noosa Queensland Australia. (Compiled by Dungey H. S. Dieters M. J. and Nikles D. G.) Department of Primary Industries Brisbane pp 519-525

  • Varghese M Ravi N Son SG Lindgren D (2003) Variation in fertility and its impact on gene diversity in a seedling seed orchard of Eucalyptus tereticornis In: Wei RP Xu D (eds) Eucalyptus Plantations - Research Management and Development. World Scientific Singapore pp 111-126.

  • Varghese M Harwood CE Bush DJ Baltunis B Kamalakannan R Suraj PG Hegde D Meder R (2017) Growth and wood properties of natural provenances local seed sources and clones of Eucalyptus camaldulensis in southern India: implications for breeding and deployment. New For. 48(1):67-82.

  • Varghese M Harwood CE Hegde R Ravi N (2008) Evaluation of provenances of Eucalyptus camaldulensis and clones of E. camaldulensis and E. tereticornis at contrasting sites in southern India. Silvae Genet 57:170–179.

  • Varghese M Kamalakannan R Harwood CE Lindgren D McDonald MW (2009) Changes in growth performance and fecundity of Eucalyptus camaldulensis and E. tereticornis during domestication in southern India. Tree Genet Genomes 5(4): 629-640.

  • Varghese M Nicodemus A Nagarajan B Lindgren D (2006) Impact of fertility variation on gene diversity and drift in two clonal seed orchards of teak (Tectona grandis Linn. f.). New For. 31: 497–512.

  • White DA McGrath JF Ryan MG Battaglia M Mendham DS Kinal J Downes GM Crombie DS Hunt ME (2014) Managing for water-use efficient wood production in Eucalyptus globulus plantations. For Ecol Manag 331:272–280.

  • Williams CG Savolainen O (1996) Inbreeding depression in conifers: Implications for breeding strategy. Forest Science 42:102–117.

  • Zhang L Huanqiong N Gapare WJ Dillon SK Li X Wu HX (2014) Comparison of allelic diversity between native gene resource plantings and selections in open-pollinated progeny test of Pinus radiata D. Don. Silvae Genet 63(5): 213-221.

  • Zelener N Poltri SN Bartoloni N Lopez CR Hopp HE (2005) Selection strategy for a seedling seed orchard design based on trait selection index and genomic analysis by molecular markers: a case study for Eucalyptus dunnii. Tree Physiol 25:1457–1467.

  • Zhu Y Wu S Xu J Lu Z Li G Hu Y Yang X Bush D (2017) Genetic parameters for growth traits and stem-straightness in Eucalyptus urophylla x E. camaldulensis hybrids from a reciprocal mating design. Euphytica (2017) 213:142.

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