Abstract
Herbivory on hybrid plants has the potential to affect patterns of plant evolution, such as limiting gene-flow through hybrids, and can also affect herbivore biodiversity. However, few studies have surveyed multiple hybrid species to identify phylogenetic patterns in the inheritance of plant traits that may drive herbivory. We surveyed 15 leaf traits and patterns of chewing, mining, and galling herbivory in a common garden of 17 artificially crossed hybrid oak species and each of their parental species over a 2-year period. Using a phylogeny of oaks, we tested whether hybrids that resulted from more divergent parents received more herbivory than those derived from closely related parents (as would be predicted by a build-up of incompatibilities in defensive systems over evolutionary time) and found only marginal evidence in support of this. We found that chewing damage to hybrids was weakly predicted by the relatedness of a parental species to the single native oak. The levels of chewing and mining herbivory on hybrids were typically intermediate to those of their parental species, though less than the parental mean for chewing damage in 2008. Most leaf traits of hybrids were also intermediate to those of their parental species. There was no clear pattern in terms of an association between 11 species of cynipid gall wasps and hybrids. The patterns of (1) intermediate levels of herbivory on hybrids and (2) no trend in herbivory on hybrids based on the phylogenetic relatedness of parental species suggest that herbivory may not play a general role in limiting hybrid fitness (and thus gene-flow through hybrids) in oaks.
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References
Aguilar JM, Boecklen WJ (1992) Patterns of herbivory in the Quercus grisea × Quercus gambelii species complex. Oikos 64:498–504
Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents. Trends Ecol Evol 10:67–71
Boecklen WJ, Spellenberg R (1990) Structure of herbivore communities in 2 oak (Quercus spp.) hybrid zones. Oecologia 85:92–100
Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52
Cottam WP, Tucker JM, Santamour FS (1982) Oak hybridization at the University of Utah. State Arboretum of Utah, University of Utah, Salt Lake City
Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381
Dobzhansky T (1936) Studies on hybrid sterility. II Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21:113–135
Dobzhansky T (1970) Genetics of the evolutionary process. Columbia University Press, New York
Dodd RS, Afzal-Rafii Z (2004) Selection and dispersal in a multispecies oak hybrid zone. Evolution 58:261–269
Dungey HS, Potts BM, Whitham TG, Li HF (2000) Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54:1938–1946
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608
Feeny PP (1976) Plant apparency and chemical defense. Recent Adv Phytochem 10:1–40
Floate KD, Whitham TG (1993) The hybrid bridge hypothesis—host shifting via plant hybrid swarms. Am Nat 141:651–662
Fritz RS (1999) Resistance of hybrid plants to herbivores: genes, environment, or both? Ecology 80:382–391
Fritz RS, Nicholsorians CM, Brunsfeld SJ (1994) Interspecific hybridization of plants and resistance to herbivores—hypotheses, genetics, and variable responses in a diverse herbivore community. Oecologia 97:106–117
Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Ann Rev Ecol Syst 30:565–591
Graham DH (1992) Stabilization of the Prussian blue color in the determination of polyphenols. J Agric Food Chem 40:801–805
Grant V (1971) Plant speciation. Columbia University Press, New York
Hagerman AE (1987) Radial diffusion method for determining tannin in plant-extracts. J Chem Ecol 13:437–449
Hanhimaki S, Senn J, Haukioja E (1994) Performance of insect herbivores on hybridizing trees—the case of the sub-arctic birches. J Anim Ecol 63:163–175
Hipp AL, Weber JA (2008) Taxonomy of Hill’s oak (Quercus ellipsoidalis: Fagaceae): evidence from AFLP data. Syst Bot 33:148–158
Howard DJ, Preszler RW, Williams J, Fenchel S, Boecklen WJ (1997) How discrete are oak species? Insights from a hybrid zone between Quercus grisea and Quercus gambelii. Evolution 51:747–755
Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.71. Available at: http://mesquiteproject.org
McIntyre PJ, Whitham TG (2003) Plant genotype affects long-term herbivore population dynamics and extinction: conservation implications. Ecology 84:311–322
Moorehead JR, Taper ML, Case TJ (1993) Utilization of hybrid oak hosts by a monophagous gall wasp—how little host character is sufficient. Oecologia 95:385–392
Moulia C, Aussel JP, Bonhomme F, Boursot P, Nielsen JT, Renaud F (1991) Wormy mice in a hybrid zone—a genetic-control of susceptibility to parasite infection. J Evol Biol 4:679–687
Nason JD, Ellstrand NC, Arnold ML (1992) Patterns of hybridization and introgression in populations of oaks, manzanitas, and irises. Am J Bot 79:101–111
Orians CM (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
Orians CM, Fritz RS (1995) Secondary chemistry of hybrid and parental willows—phenolic glycosides and condensed tannins in Salix sericea, S. eriocephala, and their hybrids. J Chem Ecol 21:1245–1253
Paradis E, Claude J, Strimmer K (2004) APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. Proc Natl Acad Sci USA 106:18097–18102
Pearse IS, Krugel T, Baldwin IT (2006) Innovation in anti-herbivore defense systems during neopolypoloidy—the functional consequences of instantaneous speciation. Plant J 47:196–210
Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230
R Core Development Team (2009) R: A language and environment for statistical computing, reference index version 2.8.1. R Foundation for Statistical Computing, Vienna, Austria.
Rhode JM, Cruzan MB (2005) Contributions of heterosis and epistasis to hybrid fitness. Am Nat 166:E124–E139
Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389
Roslin T, Salminen JP (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117:1560–1568
Russo R (2006) Field guide to plant galls of California and other western states. University of California Press, Berkeley
Stone GN, Schonrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668
Strauss SY (1994) Levels of herbivory and parasitism in host hybrid zones. Trends Ecol Evol 9:209–214
Tovar-Sanchez E, Oyama K (2006a) Community structure of canopy arthropods associated to Quercus crassifolia × Quercus crassipes complex. Oikos 112:370–381
Tovar-Sanchez E, Oyama K (2006b) Effect of hybridization of the Quercus crassifolia × Quercus crassipes complex on the community structure of endophagous insects. Oecologia 147:702–713
Vila M, D’Antonio CM (1998) Hybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal California. Ecol Appl 8:1196–1205
Whitham TG (1989) Plant hybrid zones as sinks for pests. Science 244:1490–1493
Williams JH, Boecklen WJ, Howard DJ (2001) Reproductive processes in two oak (Quercus) contact zones with different levels of hybridization. Heredity 87:680–690
Yarnes CT, Boecklen WJ, Salminen JP (2008) No simple sum: seasonal variation in tannin phenotypes and leaf-miners in hybrid oaks. Chemoecology 18:39–51
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Communicated by Diethart Matthies.
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Pearse, I.S., Baty, J.H. The predictability of traits and ecological interactions on 17 different crosses of hybrid oaks. Oecologia 169, 489–497 (2012). https://doi.org/10.1007/s00442-011-2216-5
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DOI: https://doi.org/10.1007/s00442-011-2216-5