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Inheritance Of Resistance to Mammalian Herbivores and of Plant Defensive Chemistry in an Eucalyptus Species

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Abstract

Hybridization in plants provides an opportunity to investigate the patterns of inheritance of hybrid resistance to herbivores, and of the plant mechanisms conferring this resistance such as plant secondary metabolites. We investigated how inter-race differences in resistance of Eucalyptus globulus to a generalist mammalian herbivore, Trichosurus vulpecula, are inherited in their F1 hybrids. We assessed browsing damage of 3-year-old trees in a common environment field trial on four hybrid types of known progeny. The progeny were artificial intra-race crosses and reciprocal inter-race F1 hybrids of two geographically distinct populations (races) of E. globulus north-eastern Tasmania and south-eastern Tasmania. Populations of trees from north-eastern Tasmania are relatively susceptible to browsing by T. vulpecula, while populations from south-eastern Tasmania are more resistant. We assessed the preferences of these trees in a series of paired feeding trials with captive animals to test the field trial results and also investigated the patterns of inheritance of plant secondary metabolites. Our results demonstrated that the phenotypic expression of resistance of the inter-race F1 hybrids supported the additive pattern of inheritance, as these hybrids were intermediate in resistance compared to the pure parental hybrids. The expression of plant secondary metabolites in the F1 hybrids varied among major groups of individual compounds. The most common pattern supported was dominance towards one of the parental types. Together, condensed tannins and essential oils appeared to explain the observed patterns of resistance among the four hybrid types. While both chemical groups were inherited in a dominant manner in the inter-race F1 hybrids, the direction of dominance was opposite. Their combined concentration, however, was inherited in an additive manner, consistent with the phenotypic differences in browsing.

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References

  • Abbott, I., Vanheurck, P., Burbidge, T., and Williams, M. 1993. Damage caused by insects and fungi to eucalypt foliage-spatial and temporal patterns in mediterranean forest of Western Australia. For. Ecol. Manage. 58:85–110.

    Google Scholar 

  • Aguilar, J. M. and Boecklen, W. J. 1992. Patterns of herbivory in the Quercus grisea × Quercus gambelii species complex. Oikos 64:498–504.

    Google Scholar 

  • Anderson, L. L. and Paige, K. N. 2003. Multiple herbivores and coevolutionary interactions in an Ipomopsis hybrid swarm. Evol. Ecol. 17:139–156.

    Google Scholar 

  • Bailey, J. K., Schweitzer, J. A., Rehill, B. J., Lindroth, R. L., Martinsen, G. D., and Whitham, T. G. 2004. Beavers as molecular geneticists: A genetic basis to the foraging of an ecosystem engineer. Ecology 85:603–608.

    Google Scholar 

  • Boecklen, W. J. and Spellenberg, R. 1990. Structure of herbivore communities in two oak (Quercus spp.) hybrid zones. Oecologia 85:92–100.

    Google Scholar 

  • Bulinski, J. and McArthur, C. 1999. An experimental field study of the effects of mammalian herbivore damage on Eucalyptus nitens seedlings. For. Ecol. Manage. 113:241–249.

    Google Scholar 

  • Byrd, D. W., McArthur, E. D., Wang, H., Graham, J. H., and Freeman, D. C. 1999. Narrow hybrid zone between two subspecies of big sagebrush, Artemisia tridentata (Asteraceae). VIII. Spatial and temporal pattern of terpenes. Biochem. Syst. Ecol. 27:11–25.

    Google Scholar 

  • Close, D. C., McArthur, C., Paterson, S., Fitzgerald, H., Walsh, A., and Kincade, T. 2003. Photoinhibition: A link between effects of the environment on eucalypt seedling leaf chemistry and herbivory. Ecology 84:2952–2966.

    Google Scholar 

  • Dungey, H. S. and Potts, B. M. 2002. Susceptibility of some Eucalyptus species and their hybrids to possum damage. Aust. For. 65:23–30.

    Google Scholar 

  • Dungey, H. S. and Potts, B. M. 2003. Eucalypt hybrid susceptibility to Gonipterus scutellatus (Coleoptera: Curculionidae). Aust. Ecol. 28:70–74.

    Google Scholar 

  • Dungey, H. S., Potts, B. M., Whitham, T. G., and Li, H.-F. 2000. Plant genetics affects arthropod community richness and composition: Evidence from a synthetic eucalypt hybrid population. Evolution 54:1938–1946.

    CAS  PubMed  Google Scholar 

  • Dutkowski, G. W. and Potts, B. M. 1999. Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification. Aust. J. Bot. 47:237–263.

    Google Scholar 

  • Eisenbach, J. 1996. Three-trophic-level interactions in cattail hybrid zones. Oecologia 105:258–265.

    Google Scholar 

  • Eschler, B. M., Pass, D. M., Willis, R., and Foley, W. J. 2000. Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biol. Syst. Ecol. 28:813–824.

    Google Scholar 

  • Eyles, A., Davies, N. W., and Mohammed, C. 2003. Novel detection of formylated phloroglucinol compounds (FPCs) in the wound wood of Eucalyptus globulus and E. nitens. J. Chem. Ecol. 29:881–898.

    Google Scholar 

  • Floate, K. D., Kearsley, M. J. C., and Whitham, T. G. 1993. Elevated herbivory in plant hybrid zones: Chrysomela confluens, Populus and phonological sinks. Ecology 74:2056–2065.

    Google Scholar 

  • Fritz, R. S. 1999. Resistance of hybrid plants to herbivores: Genes, environment, or both? Ecology 80:382–391.

    Google Scholar 

  • Fritz, R. S. 2001. Plant hybrids. Enc. Biodivers. 4:659–675.

    Google Scholar 

  • Fritz, R. S., Hochwender, C. G., Lewkiewicz, D. A., Bothwell, S., and Orians, C. M. 2001. Seedling herbivory by slugs in a willow hybrid system: Developmental changes in damage, chemical defense, and plant performance. Oecologia 129:87–97.

    Article  Google Scholar 

  • Fritz, R. S., Roche, B. M., and Brunsfeld, S. J. 1998. Genetic variation in resistance of hybrid willows to herbivores. Oikos 83:117–128.

    Google Scholar 

  • Fritz, R. S., Roche, B. M., Brunsfeld, S. J., and Orians, C. M. 1996. Interspecific and temporal variation in herbivore responses to hybrid willows. Oecologia 108:121–129.

    Google Scholar 

  • Gange, A. C. 1995. Aphid performance in an alder (Alnus) hybrid zone. Ecology 76:2074–2083.

    Google Scholar 

  • Gilbert, J. M. 1961. The effects of browsing by native animals on the establishment of seedlings of Eucalyptus regnans in the Florentine Valley, Tasmania. Aust. For. 25:116–121.

    Google Scholar 

  • Graham, H. D. 1992. Stabilization of the Prussian blue color in the determination of polyphenols. J. Agric. Food Chem. 40:801–805.

    Google Scholar 

  • Hagerman, A. E. 1995. Tannin Analysis, 2nd edn. Miami University, Oxford, OH.

    Google Scholar 

  • Hagerman, A. E. and Butler, L. G. 1991. Tannins and lignins, pp. 355–388, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Vol. 1. The Chemical Participants. Academic, San Diego, CA.

    Google Scholar 

  • Hallgren, P., Ikonen, A., Hjalten, J., and Roininen, H. 2003. Inheritance patterns of phenolics in Fl, F2, and back-cross hybrids of willows: Implications for herbivore responses to hybrid plants. J. Chem. Ecol. 29:1143–1158.

    Google Scholar 

  • Harborne, J. B. 1991. The chemical basis of plant defense, pp. 45–59, in R. T. Palo and C. T. Robbins (eds.). Plant Defenses Against Mammalian Herbivores. CRC, Boca Raton, FL.

    Google Scholar 

  • Hjältén, J. 1997. Willow hybrids and herbivory: A test of hypotheses of phytophage response to hybrid plants using the generalist leaf-feeder Lochmaea caprea (Chrysomelidae). Oecologia 109:571–574.

    Google Scholar 

  • Hjältén, J., Ericson, L., and Roininen, H. 2000. Resistance of Salix caprea, S. phylicifolia, and their Fl hybrids to herbivores and pathogens. Écoscience 7:51–56.

    Google Scholar 

  • Hume, I. and Esson, C. 1993. Nutrients, antinutrients and leaf selection by captive koalas (Phascolarctos cinereus). Aust. J. Zool. 41:379–392.

    Google Scholar 

  • James, S. A. and Bell, D. T. 2001. Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus ssp globulus (Myrtaceae). Aust. J. Bot. 49:259–269.

    Google Scholar 

  • Jordan, G. J., Potts, B. M., Chalmers, P., and Wiltshire, R. J. E. 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.

    Google Scholar 

  • Kearsley, M. J. C. and Whitham, T. G. 1989. Developmental changes in resistance to herbivory— Implications for individuals and populations. Ecology 70:422–434.

    Google Scholar 

  • Landsberg, J. 1987. Feeding preferences of common brushtail possums, Trichosurus vulpecula, on seedlings of a woodland eucalypt. Aust. Wild. Res. 14:361–369.

    Google Scholar 

  • Lawler, I. R. and Foley, W. J. 1999. Swamp wallabies and Tasmanian pademelons show intraspecific preferences for foliage. Aust. For. 62:17–20.

    Google Scholar 

  • Lawler, I. R., Foley, W. J., and Eschler, B. M. 2000. Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81:1327–1338.

    Google Scholar 

  • Lawrence, R., Potts, B. M., and Whitham, T. G. 2003. Relative importance of plant ontogeny, host genetic variation, and leafage for a common herbivore. Ecology 84:1171–1178.

    Google Scholar 

  • Lowther, J. R. 1980. Use of a single sulphuric acid-hydrogen peroxide digest for the analysis of Pinus radiata needles. Comm. Soil Sci. Plant Anal. 11:178–188.

    Google Scholar 

  • Marquis, R. J. 1990. Genotypic variation in leaf damage in Piper arieianum (Piperaceae) by a multispecies assemblage of herbivores. Evolution 44:104–120.

    Google Scholar 

  • Marsh, K. J., Wallis, I. R., and Foley, W. J. 2003. The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore (Pseudocheirus peregrinus) and a generalist herbivore (Trichosurus vulpecula). Aust. J. Zool. 51:31–42.

    Google Scholar 

  • Mauricio, R. and Rausher, M. D. 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defence. Evolution 51:1435–1444.

    Google Scholar 

  • McArthur, C., Goodwin, A., and Turner, S. 2000. Preferences, selection and damage to seedlings under changing availability by two marsupial herbivores. For. Ecol. Manage. 139:157-173.

    Google Scholar 

  • McArthur, C. and Sanson, G. D. 1993. Nutritional effects and costs of a tannin in a grazing and a browsing macropodid marsupial herbivore. Fund. Ecol. 7:690–696.

    Google Scholar 

  • McArthur, C., Sanson, G. D., and Deal, A. M. 1995. Salivary proline-rich proteins in mammals: Roles in oral homeostasis and counteracting dietary tannin. J. Chem. Ecol. 21:663–691.

    Google Scholar 

  • O’reilly-Wapstra, J. M., McArthur, C., and Potts, B. M. 2002. Genetic variation in resistance of Eucalyptus globulus to marsupial browsers. Oecologia 130:289–296.

    Google Scholar 

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

    Google Scholar 

  • Orians, C. M. 2000. The effects of hybridization in plants on secondary chemistry: Implications for the ecology and evolution of plant–herbivore interactions. Am. J. Bot. 87:1749-1756.

    Google Scholar 

  • Orians, C. M. and Floyd, T. 1997. The susceptibility of parental and hybrid willows to plant enemies under contrasting soil and nutrient conditions. Oecologia 109:407–413.

    Google Scholar 

  • Porter, L. J., Hrstich, L. N., and Chan, B. G. 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230.

    Article  CAS  Google Scholar 

  • Scott, S. L., McArthur, C., Potts, B. M., and Joyce, K. 2002. Possum browsing—The downside to a eucalypt hybrid developed for frost tolerance in plantation forestry. For. Ecol. Manage. 157:231–245.

    Google Scholar 

  • Steinbauer, M. J. 2002. Oviposition preference and neonate performance of Mnesampela privata in relation to heterophylly in Eucalyptus dunni and E. globulus. Agric. For. Entomol. 4:245–253.

    Google Scholar 

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

    Google Scholar 

  • Strauss, S. Y. 1994. Levels of herbivory and parasitism in host hybrid zones. Tree 9:209–214.

    Google Scholar 

  • Vila, M. and D’antonio, C. M. 1998. Hybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal California. Ecol. App. 8:1196–1205.

    Google Scholar 

  • Volker, P. W. and Orme, R. W. 1988. Locality trials of Eucalyptus globulus and related species in Tasmania. Aust. For. 51:257–265.

    Google Scholar 

  • Wallis, I. R., Herlt, A. J., Eschler, B. M., Takasaki, M., and Foley, W. J. 2003. Quantification of sideroxylonals in Eucalyptus foliage by high-performance liquid chromatography. Phytochem. Anal. 14:360–365.

    Google Scholar 

  • Wallis, I. R., Watson, M. L., and Foley, W. J. 2002. Secondary metabolites in Eucalyptus melliodora: Field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum. Aust. J. Zool. 50:507–519.

    Google Scholar 

  • Whitham, T. G., Morrow, P. A., and Potts, B. M. 1994. Plant hybrid zones as centers of biodiversity: The herbivore community of two endemic Tasmanian eucalypts. Oecologia 97:481–490.

    Google Scholar 

  • Wiggins, N. L., McArthur, C., McLean, S., and Boyle, R. 2003. Effects of two plant secondary metabolites, cineole and gallic acid, on nightly feeding patterns of the common brushtail possum. J. Chem. Ecol. 29:1423–1441.

    Google Scholar 

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Authors and Affiliations

  1. School of Zoology, CRC for Sustainable Production Forestry, University of, Tasmania, Private Bag 5, Hobart, Tasmania, 7001, Australia

    Julianne M. O’REILLY-WAPSTRA & Clare Mcarthur

  2. School of Plant Science, CRC for Sustainable Production Forestry, University of Tasmania, Private Bag 55, Hobart, 7001, Tasmania, Australia

    Brad M. Potts & Paul Tilyard

  3. Central Science Laboratory, University of Tasmania, Private Bag 74, Hobart, 7001, Tasmania, Australia

    Noel W. Davies

  4. School of Plant Science, CRC for Sustainable Production Forestry, University of Tasmania, Private Bag 55, Hobart, 7001, Tasmania, Australia

    Clare Mcarthur

  5. School of Biological Sciences, The University of Sydney New South Wales, 2006, Australia

    Julianne M. O’REILLY-WAPSTRA

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  1. Julianne M. O’REILLY-WAPSTRA
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  2. Brad M. Potts
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Correspondence to Julianne M. O’REILLY-WAPSTRA.

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O’REILLY-WAPSTRA, J.M., Potts, B.M., Mcarthur, C. et al. Inheritance Of Resistance to Mammalian Herbivores and of Plant Defensive Chemistry in an Eucalyptus Species. J Chem Ecol 31, 357–375 (2005). https://doi.org/10.1007/s10886-005-1346-9

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