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Effect of hybridization of the Quercus crassifolia×Quercus crassipes complex on the community structure of endophagous insects

  • Community Ecology
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Abstract

In a previous study, we showed that the geographic proximity of hybrid plants to the allopatric areas of parental species increases their morphological and genetic similarity with them. In the present work, we explored whether the endophagous fauna of hybrid plants show the same pattern. We studied the canopy species richness, diversity and composition of leaf-mining moths (Lepidoptera: Tischeridae, Citheraniidae) and gall-forming wasps (Hymenoptera: Cynipidae) associated with two species of red oaks (Quercus crassifolia and Quercus crassipes) and their interspecific hybrid (Quercus×dysophylla Benth pro sp.) in seven hybrid zones in central Mexico, during four seasons in 2 years. The study was conducted on 194 oak trees with known genetic status [identified by leaf morphology and molecular markers (random amplified polymorphic DNAs)], and the results indicate a bidirectional pattern of gene flow. Hybrid plants supported intermediate levels of infestation of gall-forming and leaf-mining insects compared to their putative parental species. The infestation level of leaf-mining insects varied significantly following the pattern: Q. crassifolia>hybrids>Q. crassipes, whereas the gall-forming insects showed an inverse pattern. A negative and significant relationship was found between these two types of insect guilds in each host taxa, when the infestation percentage was evaluated. It was found that 31.5% (n=11) of the endophagous insects were specific to Q. crassipes, 22.9% (n=8) to Q. crassifolia, and 8.6% (n=3) to hybrid individuals. The hybrid bridge hypothesis was supported in the case of 25.7% (n=9) of insects, which suggests that the presence of a hybrid intermediary plant may favor a host herbivore shift from one plant species to another. Greater genetic diversity in a hybrid zone is associated with greater diversity in the endophagous community. The geographic proximity of hybrid plants to the allopatric site of a parental species increases their similarity in terms of endophagous insects and the Eje Neovolcánico acts as a corridor favoring this pattern.

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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

    Article  Google Scholar 

  • Anderson E (1949) Introgressive hybridization. Wiley, New York

    Google Scholar 

  • Ananthakrisham NT (1984) The biology of gall insects. Arnold, London

    Google Scholar 

  • Bacilieri R, Ducousso A, Kremer A (1995) Genetic, morphological, ecological and phenological differentiation between Quercus petrea (Matt.) Liebl. and Quercus robur L. in a hybrid zone of the northwest. Silvae Genet 44:1–1

    Google Scholar 

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

    Article  Google Scholar 

  • Boecklen WJ, Larson KC (1994) Gall-forming wasp (Hymenoptera: Cynipidae) in an oak hybrid zone: testing hypotheses about hybrid susceptibility to herbivores. In: Price PW, Mattson WJ, Baranchikov YN (eds) The ecology and evolution of gall-forming insects. North Central Forest Experimental Station, Forest Service, USDA, St. Paul, Min., pp 110–120

    Google Scholar 

  • Bruschi P, Vendramin GG, Bussotti F, Grossoni P (2000) Morphological and molecular differentiation between Quercus petrea (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in northern and central Italy. Ann Bot 85:325–333

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Connor EF, Faeth SH, Simberloff D (1983) Leaf-miners on oaks: the role of immigration in situ reproductive recruitment. Ecology 64:191–204

    Article  Google Scholar 

  • Cornell HV (1986) Oak species attributes and host size influence cynipine wasp species richness. Ecology 67:1582–1592

    Article  Google Scholar 

  • Cornell HV, Washburn JO (1979) Evolution of the richness-area correlation for cynipid gall wasp on oak tree: a comparison of two geographic areas. Evolution 33:257–274

    Article  Google Scholar 

  • Dumolin-Lapeguè S, Demesure B, Fineschi S, LeCorre V, Petit RJ (1997) Phylogeographic structure of white oaks throughout the European Continent. Genetics 146:1475–1487

    PubMed  Google Scholar 

  • Dungey HS, Potts BM, Whitham TG, Li HF (2000) Plant genetics effects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54:1938–1946

    PubMed  CAS  Google Scholar 

  • Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetation 69:57–68

    Article  Google Scholar 

  • Ferrusquía-Villafranca I (1993) Geology of Mexico: a synopsis. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico: origins and distribution. Oxford University Press, New York, pp 3–107

    Google Scholar 

  • Floate KD, Whitham TG (1993) The “hybrid bridge” hypothesis: host shifting via plant hybrid swarms. Am Nat 141:651–662

    Article  CAS  PubMed  Google Scholar 

  • Fritz RS, Simms EL (1992) Plant resistance to herbivores and phatogens. University of Chicago Press, Chicago, Ill.

    Google Scholar 

  • Fritz RS, Nichols-Orians CM, Brunsfeld SJ (1994) Interspecific hybridization of plants and resistance to herbivores: hypothesis, genetics, and variable responses in a diverse herbivore community. Oecologia 97:106–117

    Article  Google Scholar 

  • Fritz RS, Roche BM, Brunsfeld SJ, Orians CM (1996) Interspecific and temporal variation in herbivores responses to hybrid willows. Oecologia 108:121–129

    Article  Google Scholar 

  • Fritz RS, Roche BM, Brunsfeld SJ (1998) Genetic variation in resistance of hybrid willows to herbivores. Oikos 83:117–128

    Article  Google Scholar 

  • Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annu Rev Ecol Syst 30:565–591

    Article  Google Scholar 

  • Grant V (1981) Plant speciation. 2nd edn. Columbia University Press, New York

    Google Scholar 

  • Guttman SI, Weight LA (1989) Electrophoretic evidence of relationships among Quercus (oaks) of eastern North America. Can J Bot 67:339–351

    Article  Google Scholar 

  • Hall RW, Towsend AM (1987) Suitability of Ulmus wilsoniana, the “urban” elm, and their hybrids for the elm leaf beetle, Xanthogaleruca luteola (Müller) (Coleoptera: Chrysomelidae). Environ Entomol 16:1042–1044

    Google Scholar 

  • Hanhimäki S, Senn J, Haukioja E (1994) Permanence of insect herbivores on hybridizing trees: the case of the subarctic birches. J Anim Ecol 63:163–175

    Article  Google Scholar 

  • Hardin JW (1975) Hybridization and introgression in Quercus alba. J Arnold Arbor 56:336–363

    Google Scholar 

  • Jensen RJ, Eshbaugh WH (1976) Numerical taxonomic studies of hybridization in Quercus. Populations of restricted aerial distribution and low taxonomic diversity. Syst Bot 1:1–10

    Article  Google Scholar 

  • Knops JMH, Tilman D, Haddad NM, Naeem S, Mitchell CE, Haarstad J (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundance and diversity. Ecol Lett 2:286–293

    Article  Google Scholar 

  • Lawton JH (1978) Host-plant influences on insect diversity: the effects of space and time. Symp R Entomol Soc Lond 9:105–125

    Google Scholar 

  • Messina FJ, Richards JH, McArthur ED (1996) Variable responses of insects to hybrid versus parental sagebrush in common gardens. Oecologia 107:513–521

    Article  Google Scholar 

  • Moorehead JR, Taper ML, Case TJ (1993) Utilization of hybrid oak hosts by a monophaghous gall wasp: how little host character is sufficient? Oecologia 95:385–392

    Article  Google Scholar 

  • Morrow PA, Whitham TG, Potts BM, Ladiges P, Ashton DH, Williams J (1994) Gall-forming insects concentrate on hybrid phenotypes of Eucalyptus host. In: Price PW, Mattson WJ Jr, Baranchikov YN (eds) The ecology and evolution of gall-forming insects. North Central Forest Experimental Station, Forest Service, USDA, St. Paul, Min.

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nixon KC (1993) The genus Quercus in Mexico. In: Nixon KC (ed) Biological diversity of Mexico: origins and distributions, Oxford University Press, New York, pp 447–458

    Google Scholar 

  • Orians CM, Fritz RS (1995) Secundary 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289–1313

    Article  PubMed  CAS  Google Scholar 

  • Price PW, Abrahamson WG, Hunter MD, Melika G (2004) Using gall wasp on oaks to test broad ecological concepts. Conserv Biol 18:1405–1416

    Article  Google Scholar 

  • Rieseberg LH, Brunsfeld SJ (1992) Molecular evidence and plant introgression. In: Soltis PS, Soltis DE, Doyle JD (eds) Molecular systematic of plants. Chapman and Hall, New York, pp 151–176

    Google Scholar 

  • Rieseberg LH, Elltrand NC (1993) What can molecular and morphological markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241

    Article  CAS  Google Scholar 

  • Rieseberg LH, Wendel JF (1993) Introgression and its consequences in plants. In: Harrison RG (ed) hybrid zones and the evolutionary process, Oxford University Press, Oxford, pp 70–109

  • Romero RS (1993) El género Quercus (Fagaceae) en el Estado de México. M.Sc. thesis, Universidad Nacional Autónoma de México

  • Rowell-Rahier M (1984) The food plant preferentes of Phratora vitellinae (Coleoptera: Chrysomelinae). Oecologia 64:375–380

    Article  Google Scholar 

  • Shoonhoven LM, Jermy T, Van Loon JJA (1998) Insect–plant biology: from physiology to evolution. Chapman and Hall, London

    Google Scholar 

  • Simberloff D, Stiling P (1987) Larval dispersion and survivorship in a leaf-mining moth. Ecology 68:1647–1657

    Article  Google Scholar 

  • Simms EL, Rausher MD (1993) Patterns of selection on phytophage resistance in Ipomoea purpurea. Evolution 47:970–976

    Article  Google Scholar 

  • Slansky F, Scriber JM (1985) Food composition and utilization. In: Kerkurt G, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon, Oxford, pp 87–163

    Google Scholar 

  • Soetens P, Rowell-Rahier M, Pasteels JM (1991) Influence of phenolglucosides and trichome density on the distribution of insects herbivores on willows. Entomol Exp Appl 59:175–187

    Article  CAS  Google Scholar 

  • Stace CA (1987) Hybridization and the plant species. In: Urbanska KM (ed) Differentiation patterns in higher plants. Academic Press, New York, pp 115–127

    Google Scholar 

  • Stone GN, Schönrogge K, Atkinson RJ, Pujade-Villar J (2002) The population biology of gall wasp (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668

    Article  PubMed  CAS  Google Scholar 

  • Strauss SY (1994) Levels of herbivory and parasitism in host hybrid zones. Trends Ecol Evol 9:209–214

    Article  Google Scholar 

  • Strong DR, Lawton JH, Southwood TRE (1984) Insects on plants: community patterns and mechanisms. Harvard University Press, Cambridge, Mass.

    Google Scholar 

  • Tovar-Sánchez E, Oyama K (2004) Natural hybridization and hybrid zones between Quercus crassifolia and Q. crassipes in Mexico. Morphological and molecular evidence. Am J Bot 91:1352–1363

    Google Scholar 

  • Warwick RM, Clarke KR, Suharsono A (1990) A statistical analysis of coral community responses to the 1982–1983 El Niño in the Thousand Island, Indonesia. Coral Reefs 8:171–179

    Article  Google Scholar 

  • Wendel LH (1960) Cynipid Galls of the Southwest. Privately printed, Ann Arbor, Mich.

  • Wendel JF, Steward JMcD, Rettig JH (1991) Molecular evidence for homoploid reticulate evolution among Australian species of Gossypium. Evolution 45:694–711

    Article  Google Scholar 

  • Whitham TG, Morrow PA, Potts BM (1994) Plant hybrid zones as center of biodiversity: the herbivore community of two endemic Tasmanian eucalypts. Oecologia 97:481–490

    Article  Google Scholar 

  • Whitham TG, Martinsen GD, Floate KD, Dungey H, Potts BM, Keim P (1999) Plant hybrid zones affect biodiversity: tools for a genetic-based understanding of community structure. Ecology 80:416–428

    Article  Google Scholar 

  • Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci USA 88:2540–2544

    Article  PubMed  CAS  Google Scholar 

  • Wimp GM, Young WP, Woolbright SA, Martinsen GD, Keim P, Whitham TG (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780

    Article  Google Scholar 

  • Wimp GM, Gregory D, Martinsen GD, Floate KD, Bangert RK, Whitham TG (2005) Plant genetic determinants of arthropod community structure and diversity. Evolution 59:61–69

    PubMed  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Englewood Cliffs, N.J.

    Google Scholar 

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Acknowledgements

We thank Jim Cronin and two anonymous reviewers for their comments that improved the original manuscript considerably. The authors thank Patricia Mussali, Susana Valencia, Rocio Esteban, Marco Romero, Mauricio Mora, and Maribel Paniagua for technical assistance. This research was supported by a PAEP–UNAM grant and a CONACYT scholarship to E. T. S.

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  1. Centro de Investigaciones en Ecosistemas, UNAM, Campus Morelia, Antigua Carretera a Pátzcuaro no. 8701, Col. San José de la Huerta, Morelia, Michoacán, México

    E. Tovar-Sánchez & K. Oyama

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  1. E. Tovar-Sánchez
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Correspondence to E. Tovar-Sánchez.

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Communicated by Jim Cronin

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Tovar-Sánchez, E., Oyama, K. Effect of hybridization of the Quercus crassifolia×Quercus crassipes complex on the community structure of endophagous insects. Oecologia 147, 702–713 (2006). https://doi.org/10.1007/s00442-005-0328-5

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