Skip to main content
SpringerLink
Log in

The Extended Community-Level Effects of Genetic Variation in Foliar Wax Chemistry in the Forest Tree Eucalyptus globulus

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Genetic variation in foundation trees can influence dependent communities, but little is known about the mechanisms driving these extended genetic effects. We studied the potential chemical drivers of genetic variation in the dependent foliar community of the focal tree Eucalyptus globulus. We focus on the role of cuticular waxes and compare the effects to that of the terpenes, a well-studied group of secondary compounds known to be bioactive in eucalypts. The canopy community was quantified based on the abundance of thirty-nine distinctive arthropod and fungal symptoms on foliar samples collected from canopies of 246 progeny from 13 E. globulus sub-races grown in a common garden trial. Cuticular waxes and foliar terpenes were quantified using gas chromatography - mass spectrometry (GC-MC). A total of 4 of the 13 quantified waxes and 7 of the 16 quantified terpenes were significantly associated with the dependent foliar community. Variation in waxes explained 22.9% of the community variation among sub-races, which was equivalent to that explained by terpenes. In combination, waxes and terpenes explained 35% of the genetic variation among sub-races. Only a small proportion of wax and terpene compounds showing statistically significant differences among sub-races were implicated in community level effects. The few significant waxes have previously shown evidence of divergent selection in E. globulus, which signals that adaptive variation in phenotypic traits may have extended effects. While highlighting the role of the understudied cuticular waxes, this study demonstrates the complexity of factors likely to lead to community genetic effects in foundation trees.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abdala-Roberts L, Mooney K (2014) Ecological and evolutionary consequences of plant genotype diversity in a tri-trophic system. Ecology 95:2879–2893

    Article  Google Scholar 

  • Axelsson E, Iason G, Julkunen-Tiitto R, Whitham T (2015) Host genetics and environment drive divergent responses of two resource sharing gall-formers on Norway spruce: a common garden analysis. PLoS One 10:e0142257

    Article  PubMed  PubMed Central  Google Scholar 

  • Bailey JK, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol Lett 9:78–85

    PubMed  Google Scholar 

  • Baker E (1982) Chemistry and morphology of plant epicuticular waxes. In: Cutler D, Alvin K, Price C (eds) The plant cuticle. Academic Press, London, pp 139–165

    Google Scholar 

  • Barbour RC, O'Reilly-Wapstra JM, De Little DW, Jordan GJ, Steane DA, Humphreys JR, Bailey JK, Whitham TG, Potts BM (2009) A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology 90:1762–1772

    Article  PubMed  Google Scholar 

  • Barbour M, Rodriguez-Cabal M, Wu E, Julkunen-Tiitto R, Ritland C, Miscampbell A, Jules E, Crutsinger G (2015) Multiple plant traits shape the genetic basis of herbivore community assembly. Funct Ecol 29:995–1006

    Article  Google Scholar 

  • Barton K, Valkama E, Vehviläinen H, Ruohomäki K, Knight T, Koricheva J (2015) Additive and non-additive effects of birch genotypic diversity on arthropod herbivory in a long-term field experiment. Oikos 124:697–706

    Article  Google Scholar 

  • Batish D, Singh H, Kohli R, Kaur S (2008) Eucalyptus essential oil as a natural pesticide. Forest Ecol Manag 256:2166–2174

    Article  Google Scholar 

  • Bodnaryk R (1992) Leaf epicuticular wax, an antixenotic factor in Brassicaceae that affects the rate and pattern of feeding of flea beetles, Phyllotreta cruciferae (Goeze). Can J Plant Sci 72:1295–1303

    Article  Google Scholar 

  • Borzak C, Potts B, Davies N, O’Reilly-Wapstra J (2014) Population divergence in the ontogenetic trajectories of foliar terpenes of a Eucalyptus species. Ann Bot-London 115:159–170

    Article  Google Scholar 

  • Brennan E, Weinbaum S (2001) Effect of epicuticular wax on adhesion of psyllids to glaucous juvenile and glossy adult leaves of Eucalyptus globulus Labillardière. Aust J Entomol 40:270–277

    Article  Google Scholar 

  • Brunet S, Jackson F, Hoste H (2008) Effects of sainfoin (Onobrychis viciifolia) extract and monomers of condensed tannins on the association of abomasal nematode larvae with fundic explants. Int J Parasitol 38:783–790

    Article  CAS  PubMed  Google Scholar 

  • Compson Z, Hungate B, Koch G, Hart S, Maestas J, Adams K, Whitham T, Marks J (2015) Closely related tree species differentially influence the transfer of carbon and nitrogen from leaf litter up the aquatic food web. Ecosystems 18:186–201

    Article  CAS  Google Scholar 

  • Compson Z, Hungate B, Whitham T, Meneses N, Busby P, Wojtowicz T, Ford A, Adams K, Marks J (2016) Plant genotype influences aquatic-terrestrial ecosystem linkages through timing and composition of insect emergence. Ecosphere 7:e01331

    Article  Google Scholar 

  • Cornelissen T, Stiling P (2006) Responses of different herbivore guilds to nutrient addition and natural enemy exclusion. Ecoscience 13:66–74

    Article  Google Scholar 

  • Crous P, Braun U, Groenewald J (2007) Mycosphaerella is polyphyletic. Stud Mycol 58:1–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeWoody J, Viger M, Lakatos F, Tuba K, Taylor G, Smulders M (2013) Insight into the genetic components of community genetics: QTL mapping of insect association in a fast-growing forest tree. PLoS One 8:e79925

    Article  PubMed  PubMed Central  Google Scholar 

  • Dungey H, Potts B, Whitham T, Li H (2000) Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54:1938–1946

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Edwards P (1982) Do waxes on juvenile Eucalyptus leaves provide protection from grazing insects? Aust J Ecol 7:347–352

    Article  Google Scholar 

  • Edwards P, Wanjura W, Brown W (1993) Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids. Oecologia 95:551–557

    Article  PubMed  Google Scholar 

  • Eigenbrode S (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthropod Struct Dev 33:91–102

    Article  CAS  PubMed  Google Scholar 

  • Eigenbrode S, Espelie K (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40:171–194

    Article  Google Scholar 

  • Eigenbrode S, Jetter R (2002) Attachment to plant surface waxes by an insect predator. Integr Comp Biol 42:1091–1099

    Article  CAS  PubMed  Google Scholar 

  • Ennis D, Despland E, Chen F, Forgione P, Bauce E (2015) Spruce budworm feeding and oviposition are stimulated by monoterpenes in white spruce epicuticular waxes. Insect Sci 00:1–8

    Google Scholar 

  • Forkner R, Marquis R, Lill J (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29:174–187

    Article  Google Scholar 

  • Gehring C, Flores-Rentería D, Sthultz C, Leonard T, Flores-Rentería L, Whipple A, Whitham T (2014) Plant genetics and interspecific competitive interactions determine ectomycorrhizal fungal community responses to climate change. Mol Ecol 23:1379–1391

    Article  PubMed  Google Scholar 

  • Glen M, Smith A, Langrell S, Mohammed C (2007) Development of nested polymerase chain reaction detection of Mycosphaerella spp. and its application to the study of leaf disease in Eucalyptus plantations. Phytopathology 97:132–144

    Article  CAS  PubMed  Google Scholar 

  • Gosney J, O'Reilly-Wapstra J, Forster L, Barbour R, Iason G, Potts B (2014) Genetic and ontogenetic variation in an endangered tree structures dependent arthropod and fungal communities. PLoS One 9:e114132

    Article  PubMed  PubMed Central  Google Scholar 

  • Gosney B, Potts B, O'Reilly-Wapstra J, Vaillancourt R, Fitzgerald H, Davies N, Freeman J (2016) Genetic control of cuticular wax compounds in Eucalyptus globulus. New Phytol 209:202–215

    Article  CAS  PubMed  Google Scholar 

  • Hamilton MG, Williams DR, Tilyard PA, Pinkard EA, Wardlaw TJ, Glen M, Vaillancourt RE, Potts BM (2013) A latitudinal cline in disease resistance of a host tree. Heredity 110:372–379

  • Heather W (1967a) Leaf characteristics of Eucalyptus Bicostata maiden et al. seedlings affecting the deposition and germination of spores of Pheoseptoria eucalypti (Hansf.). Walker. Aust J Biol Sci 20:1155–1160

    Article  Google Scholar 

  • Heather W (1967b) Susceptibility of the juvenile leaves of Eucalyptus Bicostata maiden et al. to infection by Pheoseptoria eucalypti (Hansf.). Walker. Aust J Biol Sci 20:769–775

    Article  Google Scholar 

  • Henery M, Henson M, Wallis I, Stone C, Foley W (2008) Predicting crown damage to Eucalyptus grandis by Paropsis atomaria with direct and indirect measures of leaf composition. Forest Ecol Manag 255:3642–3651

    Article  Google Scholar 

  • Hersch-Green E, Turley N, Johnson M (2011) Community genetics: what have we accomplished and where should we be going? Philos T R Soc B 366:1453–1460

    Article  Google Scholar 

  • Jarrold S, Moore D, Potter U, Charnley A (2007) The contribution of surface waxes to pre-penetration growth of an entomopathogenic fungus on host cuticle. Mycol Res 111:240–249

    Article  PubMed  Google Scholar 

  • Jones T, Potts B, Vaillancourt R, Davies N (2002) Genetic resistance of Eucalyptus globulus to autumn gum moth defoliation and the role of cuticular waxes. Can J For Res 32:1961–1969

    Article  CAS  Google Scholar 

  • Keith A, Bailey J, Whitham T (2010) A genetic basis to community repeatability and stability. Ecology 91:3398–3406

    Article  PubMed  Google Scholar 

  • Korkama-Rajala T, Müller M, Pennanen T (2007) Decomposition and fungi of needle litter from slow- and fast-growing Norway spruce (Picea abies) clones. Microb Ecol 56:76–89

    Article  PubMed  Google Scholar 

  • Külheim C, Padovan A, Hefer C, Krause ST, Köllner TG, Myburg AA, Degenhardt J, Foley WJ (2015) The eucalyptus terpene synthase gene family. BMC Genomics 16:1

    Article  Google Scholar 

  • Kunst L, Samuels A (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42:51–80

    Article  CAS  PubMed  Google Scholar 

  • Lau M, Keith A, Borrett S, Shuster S, Whitham T (2016) Genotypic variation in foundation species generates network structure that may drive community dynamics and evolution. Ecology 97:733–742

    PubMed  Google Scholar 

  • Li H, Madden J, Potts B (1997) Variation in leaf waxes of the Tasmanian Eucalyptus species - I. Subgenus Symphyomyrtus. Biochem Syst Ecol 25:631–657

    Article  Google Scholar 

  • Loch A, Floyd R (2001) Insect pests of Tasmanian blue gum, Eucalyptus globulus, in south-western Australia: history, current perspectives and future prospects. Austral Ecol 26:458–466

    Article  Google Scholar 

  • Macauley B, Fox L (1980) Variation in total phenols and condensed tannins in Eucalyptus: leaf phenology and insect grazing. Aust J Ecol 5:31–35

    Article  Google Scholar 

  • Macias F, Galindo J, Galindo J (2007) Evolution and current status of ecological phytochemistry. Phytochemistry 68:2917–2936

    Article  CAS  PubMed  Google Scholar 

  • Maddox G, Root R (1987) Resistance to 16 diverse species of herbivorous insects within a population of goldenrod, Solidago altissima: genetic variation and heritability. Oecologia 72:8–14

    Article  CAS  PubMed  Google Scholar 

  • Maldonado-Lopez Y, Cuevas-Reyes P, González-Rodríguez A, Pérez-López G, Acosta-Gómez C, Oyama K (2015) Relationships among plant genetics, phytochemistry and herbivory patterns in Quercus castanea across a fragmented landscape. Ecol Res 30:133–143

    Article  CAS  Google Scholar 

  • Matsuki M, Foley W, Floyd R (2011) Role of volatile and non-volatile plant secondary metabolites in host tree selection by christmas beetles. J Chem Ecol 37:286–300

    Article  CAS  PubMed  Google Scholar 

  • O'Reilly-Wapstra J, McArthur C, Potts B (2004) Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species. Funct Ecol 18:677–684

    Article  Google Scholar 

  • O'Reilly-Wapstra J, Freeman J, Davies N, Vaillancourt R, Fitzgerald H, Potts B (2011) Quantitative trait loci for foliar terpenes in a global eucalypt species. Tree Genet Genomes 7:485–498

    Article  Google Scholar 

  • Oyedeji A, Ekundayo O, Olawore O, Adeniyi B, Koenig W (1999) Antimicrobial activity of the essential oils of five Eucalyptus species growing in Nigeria. Fitoterapia 70:526–528

    Article  CAS  Google Scholar 

  • Park R, Keane P (1982) Leaf diseases of Eucalyptus associated with Mycosphaerella species. Transactions of the British Mycol Soc 79:101–115

    Article  Google Scholar 

  • Pérez-López G, González-Rodríguez A, Oyama K, Cuevas-Reyes P (2016) Effects of plant hybridization on the structure and composition of a highly rich community of cynipid gall wasps: the case of the oak hybrid complex Quercus magnoliifolia x Quercus resinosa in Mexico. Biodivers Conserv 25:633–651

    Article  Google Scholar 

  • Post-Beittenmiller D (1996) Biochemistry and molecular biology of wax production in plants. Annu Rev Plant Physiol 47:405–430

    Article  CAS  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rapely LP, Allen GR, Potts BM (2004) Susceptibility of Eucalyptus globulus to Mnesampela privata defoliation in relation to a specific foliar wax compound. Chemoecology 14:157–163

    Google Scholar 

  • Reisige K, Gorzelanny C, Daniels U, Moerschbacher B (2006) The C28 aldehyde octacosanal is a morphogenetically active component involved in host plant recognition and infection structure differentiation in the wheat stem rust fungus. Physiol Mol Plant P 68:33–40

    Article  CAS  Google Scholar 

  • Riederer M, Schreiber L (1995) Waxes: the transport barriers of plant cuticles. In: Hamilton R (ed) Waxes: chemistry, molecular biology and functions, vol 6. The Oily Press, Dundee, pp 130–156

    Google Scholar 

  • Robinson KM, Ingvarsson PK, Jansson S, Albrectsen BR, Kliebenstein DJ (2012) Genetic variation in functional traits influences arthropod community composition in aspen (Populus tremula L.). PLoS One 7:e37679

  • Rönnberg-Wästljung A, Åhman I, Glynn C, Widenfalk O (2006) Quantitative trait loci for resistance to herbivores in willow: field experiments with varying soils and climates. Entomol Exp Appl 118:163–174

    Article  Google Scholar 

  • Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707

    Article  CAS  PubMed  Google Scholar 

  • Schweitzer J, Madritch M, Bailey J, LeRoy C, Fischer D, Rehill B, Lindroth R, Hagerman A, Wooley S, Hart S (2008) From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005–1020

    Article  CAS  Google Scholar 

  • Sinclair F, Stone G, Nicholls J, Cavers S, Gibbs M, Butterill P, Wagner S, Ducousso A, Gerber S, Petit R (2015) Impacts of local adaptation of forest trees on associations with herbivorous insects: implications for adaptive forest management. Evol Appl 8:972–987

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith A (2006) The development of strategies for the management and research of foliar pathogens on eucalypt plantations: Using Mycosphaerella as a case study. PhD Thesis, University of Tasmania. http://eprints.utas.edu.au/378/. Accessed 3 May 2017

  • Smith AH, Pinkard EA, Stone C, Battaglia M, Mohammed CL (2005) Precision and accuracy of pest and pathogen damage assessment in young eucalypt plantations. Environ Monit Assess 111:243–256

  • Smith D, Bailey J, Shuster S, Whitham T (2011) A geographic mosaic of trophic interactions and selection: trees, aphids and birds. J Evol Biol 24:422–429

    Article  CAS  PubMed  Google Scholar 

  • Steinbauer M, Clarke A, Paterson S (1998) Changes in eucalypt architecture and the foraging behaviour and development of Amorbus obscuricornis (Hemiptera: Coreidae). Bull Entomol Res 88:641–651

    Article  Google Scholar 

  • Steinbauer M, Schiestl F, Davies N (2004) Monoterpenes and epicuticular waxes help female autumn gum moth differentiate between waxy and glossy Eucalyptus and leaves of different ages. J Chem Ecol 30:1117–1142

    Article  CAS  PubMed  Google Scholar 

  • Stone C, Bacon P (1994) Relationships among moisture stress, insect herbivory, foliar cineole content and the growth of river red gum Eucalyptus camaldulensis. J Appl Ecol 31:604–612

  • Tack A, Roslin T (2011) The relative importance of host-plant genetic diversity in structuring the associated herbivore community. Ecology 92:1594–1604

    Article  PubMed  Google Scholar 

  • Tucker D, Wallis I, Bolton J, Marsh K, Rosser A, Brereton I, Nicolle D, Foley W (2010) A metabolomic approach to identifying chemical mediators of mammal–plant interactions. J Chem Ecol 36:727–735

    Article  CAS  PubMed  Google Scholar 

  • Uppalapati S, Ishiga Y, Doraiswamy V, Bedair M, Mittal S, Chen J, Nakashima J, Tang Y, Tadege M, Ratet P (2012) Loss of abaxial leaf epicuticular wax in Medicago truncatula irg1/palm1 mutants results in reduced spore differentiation of anthracnose and nonhost rust pathogens. Plant Cell 24:353–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velmala S, Rajala T, Haapanen M, Taylor A, Pennanen T (2013) Genetic host-tree effects on the ectomycorrhizal community and root characteristics of Norway spruce. Mycorrhiza 23:21–33

    Article  CAS  PubMed  Google Scholar 

  • Whitham T, Bailey J, Schweitzer J, Shuster S, Bangert R, Leroy C, Lonsdorf E, Allan G, DiFazio S, Potts B, Fischer D, Gehring C, Lindroth R, Marks J, Hart S, Wimp G, Wooley S (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    Article  CAS  PubMed  Google Scholar 

  • Whitham T, Gehring C, Lamit L, Wojtowicz T, Evans L, Keith A, Smith D (2012) Community specificity: life and afterlife effects of genes. Trends Plant Sci 17:271–281

    Article  CAS  PubMed  Google Scholar 

  • Wimp G, Martinsen G, Floate K, Bangert R, Whitham T (2005) Plant genetic determinants of arthropod community structure and diversity. Evolution 59:61–69

    Article  PubMed  Google Scholar 

  • Wimp G, Wooley S, Bangert R, Young W, Martinsen G, Keim P, Rehill B, Lindroth R, Whitham T (2007) Plant genetics predicts intra-annual variation in phytochemistry and arthropod community structure. Mol Ecol 16:5057–5069

    Article  CAS  PubMed  Google Scholar 

  • Yarnes C, Boecklen W, Salminen J (2008) No simple sum: seasonal variation in tannin phenotypes and leaf-miners in hybrid oaks. Chemoecology 18:39–51

    Article  CAS  Google Scholar 

  • Yeats T, Rose J (2013) The formation and function of plant cuticles. Plant Physiol 163:5–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zinkgraf M, Meneses N, Whitham T, Allan G (2016) Genetic variation in NIN1 and C/VIF1 genes is significantly associated with Populus angustifolia resistance to a galling herbivore, Pemphigus betae. J Insect Physiol 84:50–59

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Paul Tilyard, and Justin Bloomfield for collection of the samples involved in this study. Tim Wardlaw and Caroline Mohammad for help in the identification of symptoms. Peter Harrison for symptom assessment. Noel Davies and Hugh Fitzgerald for the analysis and quantification of the chemistry involved in the study, and Jules Freeman and René Vaillancourt for discussion and contribution to early wax studies. Forestry Tasmania and Forico Pty Limited for access to the trials. This study is part of a PhD undertaken by Benjamin Gosney, supported by an International Postgraduate Scholarship provided by the University of Tasmania and funded by the Australian Government. Data collection was funded by Australian Research Council Discovery (DP0773686) and Linkage (LP120200380 in partnership with Greening Australia) grants.

Author information

Authors and Affiliations

  1. School of Biological Science, University of Tasmania, Private Bag 55, Hobart, TAS, 7001, Australia

    Benjamin Gosney, Julianne O’Reilly-Wapstra, Carmen Whiteley & Brad Potts

  2. School of Agricultural Science, University of Tasmania, Private Bag 50, Hobart, TAS, 7001, Australia

    Lynne Forster

  3. ARC Training Centre for Forest Value, University of Tasmania, Private Bag 55, Hobart, TAS, 7001, Australia

    Carmen Whiteley & Brad Potts

Authors
  1. Benjamin Gosney
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julianne O’Reilly-Wapstra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lynne Forster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carmen Whiteley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brad Potts
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin Gosney.

Electronic supplementary material

ESM 1

(PDF 2768 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gosney, B., O’Reilly-Wapstra, J., Forster, L. et al. The Extended Community-Level Effects of Genetic Variation in Foliar Wax Chemistry in the Forest Tree Eucalyptus globulus . J Chem Ecol 43, 532–542 (2017). https://doi.org/10.1007/s10886-017-0849-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-017-0849-5

Keywords

Search

Navigation