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Quantitative trophic networks of insect gallers and their parasitoids in the hybrid oak complex Quercus magnoliifolia x Quercus resinosa

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Abstract

Oak hybridization have important effects on the structure of herbivorous insect communities and associated natural enemies. We tested the effects of hybridization between Q. magnoliifolia and Q. resinosa on insect gallers trophic networks and their parasitoids. We characterized the genotypes of 35 individuals of Q. magnoliifolia, 30 of Q. resinosa, and 57 hybrids using eight nuclear microsatellite markers. We collected 6,798 galls from the oak hybrid complex distributed in 33 gall morphospecies on Q. magnoliifolia, 28 on Q. resinosa, and 42 on hybrid oaks. Galler-parasitoid networks were realized by 21 gall morphospecies and 21 parasitoid species for Q. magnoliifolia; 16 gall morphospecies and 30 parasitoid species for Q. resinosa; and 25 gall morphospecies and 23 parasitoid species for hybrids. Plant-galler networks were different among three oak groups, having the hybrid network higher values of diversity of interactions, nestedness and modularity and lower values of specialization than Q. magnoliifolia and Q. resinosa networks. Hybrid network of gallers and parasitoids had higher diversity of interactions, connectance and generality and lower modularity than Q. magnoliifolia and Q. resinosa networks. Hybrids are more vulnerable to insect galler incidence having low pressure by parasitoids, which allow more gall incidence in hybrid plants. Our study corroborated that hybridization generates changes in oak genetic composition influencing insect gallers trophic networks and their parasitoids. Our findings are also consistent with the rule of genetic similarity which suggest a relationship between plant genetics and the associated arthropod community, where genetically similar plants support similar arthropod communities.

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References

  • Albarrán-Lara AL, Mendoza-Cuenca L, Valencia-Avalos S, Gonzalez-Rodriguez A, Oyama K (2010) Leaf fluctuating asymmetry increases with hybridization and introgression between Quercus magnoliifolia and Quercus resinosa (Fagaceae) through an altitudinal gradient in Mexico. Int J Plant Sci 171:310–322

    Article  Google Scholar 

  • Albarrán-Lara AL, Petit RJ, Kremer A, Caron H, Peñaloza-Ramírez JM, Gugger PF, Oyama K (2019) Low genetic differentiation between two morphologically and ecologically distinct giant-leaved Mexican oaks. Plant Syst Evol 305:89–101

    Article  Google Scholar 

  • Alhmedi A, Haubruge E, D’Hoedt S, Francis F (2011) Quantitative food webs of herbivore and related beneficial community in non-crop and crop habitats. Biol Control 58:103–112

    Article  Google Scholar 

  • Almeida-Neto M, Guimaraes P, JrPR G, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239

    Article  Google Scholar 

  • Araújo WS, Maia VC (2021) Topological structure of a tritrophic network composed of host plants, gall-inducing insects and parasitoids in a restinga area in Brazil. Entomol Sci. https://doi.org/10.1111/ens.12468

    Article  Google Scholar 

  • Araújo WS, Scareli-Santos C, Guilherme FAG, Cuevas-Reyes P (2013) Comparing galling insect richness among Neotropical savannas: effects of plant richness, vegetation structure and super-host presence. Biodivers Conserv 22:1083–1094

    Article  Google Scholar 

  • Araújo WS, Freitas ÉVDD, Kollár J, Pessoa RO, Corgosinho PHC, Valério HM, Borges MAZ (2019) Host specialization in plant-galling interactions: contrasting mites and insects. Diversity 11:180

    Article  Google Scholar 

  • Arizaga S, Martínez-Cruz J, Salcedo-Cabrales M, Bello-González MA (2009) Aspectos generales de los encinos. In: Arizaga S, Cruz JM, Cabrales MS, González MAB (eds) Manual de la biodiversidad de encinos michoacanos. Secretaría de Medio Ambiente y Recursos Naturales (Semarnat). Instituto Nacional de Ecología (INESemarnat), México, pp 12–141

    Google Scholar 

  • Askew RR (1984) The biology of gall wasps. In: Ananthakrishnan TN (ed) Biology of gall insects, pp 223–271

  • Bailey JK, Schweitzer JA, Ubeda F, Koricheva J, LeRoy CJ, Madritch MD, Rehill BJ, Bangert RK, Fischer DG, Allan GJ, Whitham TG (2009) From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Philos Trans R Soc Lond, B 364:1607–1616

    Article  Google Scholar 

  • Bangert RK, Turek RJ, Martinsen GD, Wimp GM, Bailey JK, Whitham TG (2005) Benefits of conservation of plant genetic diversity on arthropod diversity. Conserv Biol 19:379–390

    Article  Google Scholar 

  • Bangert RK, Turek RJ, Rehill B, Wimp GM, Schweitzer JA, Allan GJ, Whitham TG (2006) A genetic similarity rule determines arthropod community structure. Mol Ecol 15:1379–1391

    Article  CAS  PubMed  Google Scholar 

  • Barbour MA, Fortuna MA, Bascompte J, Nicholson JR, Julkunen-Tiitto R, Jules ES, Crutsinger GM (2016) Genetic specificity of a plant–insect food web: implications for linking genetic variation to network complexity. Proc NatL Acad Sci 11:2128–2133

    Article  Google Scholar 

  • Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020

    Article  CAS  PubMed  Google Scholar 

  • Batagelj V, Mrvar A (1998) Pajek-program for large network analysis. Connections 21:47–57

    Google Scholar 

  • Borror D, DeLong DM, Charles A (1976) An introduction to the study of insects, 4th edn. Holt, Rinehart & Winston, New York

  • Carson EW, Dowling TE (2006) Influence of hydrogeographic history and hybridization on the distribution of genetic variation in the pupfishes Cyprinodon atrorus and C. bifasciatus. Mol Ecol 15:667–679

    Article  CAS  PubMed  Google Scholar 

  • Cavender-Bares J, Pahlich A (2009) Molecular, morphological, and ecological niche differentiation of sympatric sister oak species, Quercus virginiana and Q. geminata (Fagaceae). Am J Bot 96:1690–1702

    Article  PubMed  Google Scholar 

  • Chaplin-Kramer R, Kliebenstein DJ, Chiem A, Morrill E, Mills NJ, Kremen C (2011) Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators. J Appl Ecol 48:880–887

    Article  CAS  Google Scholar 

  • Cheng D, Vrieling K, Klinkhamer PGL (2011) The effect of hybridization on secondary metabolites and herbivore resistance: implications for the evolution of chemical diversity in plants. Phytochemistry Rev 10:107–117

    Article  CAS  Google Scholar 

  • Chust G, Garbin L, Pujade-Villar JULI (2007) Gall wasps and their parasitoids in cork oak fragmented forests. Ecol Entomol 32:82–91

    Article  Google Scholar 

  • Colwell RK (2009). EstimateS: statistical estimation of species richness and shared species from simples, version 8.0. http://purl.oclc.org/estimates

  • Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application published at: http://purl.oclc.org/estimates

  • Cooper WR, Rieske LK (2010) Gall structure affects ecological associations of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Environ Entomol 39:787–797

    Article  PubMed  Google Scholar 

  • Coutinho RD, Cuevas-Reyes P, Fernandes GW, Fagundes M (2019) Community structure of gall-inducing insects associated with a tropical shrub: regional, local and individual patterns. Trop Ecol 60(74):82

    Google Scholar 

  • Cronin JT, Melika G, Abrahamson WG (2020) Time-since fire and cynipid gall wasp assemblages on oaks. Biodiversity Conserv 29:1177–1203

    Article  Google Scholar 

  • Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968

    Article  CAS  PubMed  Google Scholar 

  • Cuevas-Reyes P, Canché-Delgado A, Maldonado-López Y, Fernandes GW, Oyama K, González-Rodríguez A (2018) Patterns of herbivory and leaf morphology in two Mexican hybrid oak complexes: importance of fluctuating asymmetry as indicator of environmental stress in hybrid plants. Ecol Indic 90:164–170

    Article  Google Scholar 

  • Dáttilo W, Díaz-Castelazo C, Rico-Gray V (2014) Ant dominance hierarchy determines the nested pattern in ant-plant networks. Biol J Linn Soc 113:405–414

    Article  Google Scholar 

  • de Graham MWR, V, Gijswijt MJ, (1998) Revision of the European species of Torymus Dalman (s. lat.) (Hymenoptera: Torymidae). Zoologische Verhandelingen, Leiden 317:1–202

    Google Scholar 

  • Delmas E, Besson M, Brice MH, Burkle LA, Dalla-Riva GV, Fortin MJ (2019) Analyzing ecological networks of species interactions. Biol Rev 94:16–36

    Article  Google Scholar 

  • Donatti CI, Guimaraes PR, Galetti M, Pizo MA, Marquitti FMD, Dirzo R (2011) Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecol Lett 14:773–781

    Article  PubMed  Google Scholar 

  • Dormann CF, Strauss R (2014) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98

    Article  Google Scholar 

  • Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. Interaction 1:2413793

    Google Scholar 

  • Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open J Ecol 2:7–24

    Article  Google Scholar 

  • Dreger-Jauffret F (1992) Diversity of gall-inducing insects and their galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, Oxford, pp 8–33

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Elsadany AEA, El-Metwally HA, Elabbasy EM, Agiza HN (2012) Chaos and bifurcation of a nonlinear discrete prey-predator system. Comput Ecol Softw 2:169

    Google Scholar 

  • Evans LM, Allan GJ, Whitham TG (2012) Populus hybrid hosts drive divergence in the herbivorous mite, Aceria parapopuli: implications for conservation of plant hybrid zones as essential habitat. Conserv Genet 13:1601–1609

    Article  Google Scholar 

  • Fagundes M, Xavier RCF, Faria ML, Cuevas-Reyes P, Lopes LG, Reis-Junior R (2018) Plant phenological asynchrony and community structure of gall-inducing insects in a super-host tropical tree species. Ecol Evol 8:10687–10697

    Article  PubMed  PubMed Central  Google Scholar 

  • Fagundes M, Santos ÉMS, Duarte K, Santos L, Vieira J, Oliveira C, Silva PS (2020) Diversity of gall-inducing insect associated with a superhost plant species: plant architecture, resource availability and interspecific interactions. Biodivers J Biol Divers 21:3

    Google Scholar 

  • Floate KD, Godbout J, Lau MK, Isabel N, Whitham TG (2016) Plant–herbivore interactions in a trispecific hybrid swarm of Populus: assessing support for hypotheses of hybrid bridges, evolutionary novelty and genetic similarity. New Phytol 209:832–844

    Article  CAS  PubMed  Google Scholar 

  • Fritz RS, Price PW (1988) Genetic variation among plants and insect community structure: willows and sawflies. Ecology 9:845–856

    Article  Google Scholar 

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

    Article  PubMed  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 

  • Fritz RS, Hochwender CG, Brunsfeld SJ, Roche BM (2003) Genetic architecture of susceptibility to herbivores in hybrid willows. J Evol Biol 6:1115–1126

    Article  Google Scholar 

  • Fritz RS (1992) Community Structure and Species Interactions of Phytophagous Insects on Resistant and Susceptible Host Plants. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. The University of Chicago Press, pp 240

  • Gagné RJ (1994) The gall midges of the Neotropical region. Cornell University Press, New York

    Google Scholar 

  • Gibson GAP, Huber JT, Woolley JB (1997) Annotated keys to the genera of the Nearctic Chalcidoidea (Hymenoptera). In: Gibson GAP, Huber JT, Woolley JB (eds) NRC Research Press, Ottawa, Ontario, Canada

  • González-Rodríguez A, Arias DM, Valencia S, Oyama K (2004) Morphological and RAPD analysis of hybridization between Quercus affinis and Q. laurina (Fagaceae), two mexican red oaks. Ame J Bot 91:401–409

    Article  Google Scholar 

  • Gotelli N, Colwell RK (2001) Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett. https://doi.org/10.1046/j.1461-0248.2001.00230.x

    Article  Google Scholar 

  • Graham MWR de V (1969) The Pteromalidae of north-western Europe (Hymenoptera: Chalcidoidea). Bulletin of the British Museum (Natural History) (Entomology) Supplement 16

  • Hassell MP (2000) Host parasitoid population dynamics. J Anim Ecol 69:543–566

    Article  Google Scholar 

  • Hayward A, Stone GN (2005) Oak gall wasp communities: evolution and ecology. Basic Appl Ecol 6:435–443

    Article  Google Scholar 

  • Hernández-Calderón E, González-Rodríguez A, Méndez-Alonzo R, Vega-Peña E, Oyama K (2013) Contrasting leaf phenology in two white oaks, Quercus magnoliifolia and Quercus resinosa, along an altitudinal gradient in Mexico. Can J for Res 43(2):208–213

    Article  Google Scholar 

  • Hipp AL, Manos PS, González-Rodríguez A, Hahn M, Kaproth M, McVay JD, Cavender-Bares J (2018) Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity. New Phytol 217:439–452

    Article  CAS  PubMed  Google Scholar 

  • Hirao T, Murakami M (2008) Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest. Ecol Res 23:159–168

    Article  Google Scholar 

  • Hochwender CG, Fritz RS (2004) Plant genetic differences influence herbivore community structure: evidence from a hybrid willow system. Oecologia 38:547–557

    Article  Google Scholar 

  • Hunter MD, Varley GC, Gradwell GR (1997) Estimating the relative roles of topdown and bottom-up forces on insect herbivore populations: a classic study revisited. Proc Natl Acad Sci 94:9176–9181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JH (1986) Evolution of the Fagaceae: the implications of foliar features. Ann Missouri Bot Gard 73:228–275

    Article  Google Scholar 

  • Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Ame Nat 129:657–677

    Article  Google Scholar 

  • Jordano P, Vázquez D, Bascompte J (2009) Redes complejas de interacciones mutualistas planta-animal. In: Medel R, Aizen MA, Zamora R (eds) Ecología y evolución de interacciones planta-animal. Universitaria S.A Press, Santiago de Chile, pp 17–41

    Google Scholar 

  • Kaartinen R, Roslin T (2012) High temporal consistency in quantitative food web structure in the face of extreme species turnover. Oikos 121:1771–1782

    Article  Google Scholar 

  • Keith AR, Bailey JK, Lau MK, Whitham TG (2017) Genetics-based interactions of foundation species affect community diversity, stability and network structure. Proc R Soc Lond, B 284:20162703

    Google Scholar 

  • Landi P, Minoarivelo HO, Brännström A, Hui C, Dieckmann U (2018) Complexity and stability of ecological networks: a review of the theory. Popul Ecol 60:319–345

    Article  Google Scholar 

  • Lau MK, Keith AR, Borrett SR, Shuster SM, Whitham TG (2016) Genotypic variation in foundation species generates network structure that may drive community dynamics and evolution. Ecology 97:733–742

    Article  PubMed  Google Scholar 

  • Lepais O, Gerber S (2011) Reproductive patterns shape introgression dynamics and species succession within the European white oak species complex. Int J Org Evol 65:156–170

    Article  Google Scholar 

  • Lill JT, Marquis RJ (2001) The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126:418–428

    Article  PubMed  Google Scholar 

  • Loreau MS, Naeem P, Inchausti J, Bengtsson JP, Grime A, Hector DU, Hooper MA, Huston D, Raffaelli B, Schmid D, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  CAS  PubMed  Google Scholar 

  • Losapio G, Fortuna MA, Bascompte J, Schmid B, Michalet R, Neumeyer R, Castro L, Cerretti P, Germann C, Haenni JP, Klopfstein S, Ortiz-Sanchez FJ, Pont AC, Rousse P, Schmid J, Sommaggio D, Schöb C (2019) Plant interactions shape pollination networks via nonadditive effects. Ecology 100:e02619

    Article  PubMed  Google Scholar 

  • Maldonado-López Y, Cuevas-Reyes P, Oyama K (2016) Diversity of gall wasps (Hymenoptera: Cynipidae) associated with oak trees (Fagaceae: Quercus) in a fragmented landscape in Mexico. ArthropodPlant Interact 10:29–39

    Article  Google Scholar 

  • Maldonado-López Y, Vaca-Sánchez MS, González-Rodríguez A, Oyama K, López-Barbosa E, Fagundes M, Cuevas-Reyes P (2018) Hybridization increases canopy arthropod diversity in the Quercus affinis × Quercus laurina complex. J Insect Conserv 22:781–793

    Article  Google Scholar 

  • Marquitti FMD, JrPR G, Pires MM, Bittencourt LF (2014) MODULAR: software for the autonomous computation of modularity in large network sets. Ecography 37:221–224

    Article  Google Scholar 

  • Martinsen GD, Whitham TG, Turek RJ, Keim P (2001) Hybrid populations selectively filter gene introgression between species. Evolution 55:1325–1335

    Article  CAS  PubMed  Google Scholar 

  • Mendonça JM (2007) Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal plant interaction in the neotropics. Boletin de la Sociedad Argentina de Botanica, Buenos Aires, pp 347–357

    Google Scholar 

  • Nakamura M, Asanuma M, Hiura T (2010) Differential effects of host plant hybridization on herbivore community structure and grazing pressure on forest canopies. Oikos 119:1445–1452

    Article  Google Scholar 

  • Oliveira JBBS, Maurício LF, Borges MAZ, Fagundes M, Araújo WS (2019) Comparing the plant–herbivore network topology of different insect guilds in Neotropical savannas. Ecol Entomol 45:406–415

    Article  Google Scholar 

  • Paniagua MR, Medianero E, Lewis OT (2009) Structure and vertical stratification of plant galler–parasitoid food webs in two tropical forests. Ecol Entomol 34:310–320

    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. Biodiversity Conserv 25:633–651

    Article  Google Scholar 

  • Rico-Gray V, Díaz-Castelazo C, Ramírez-Hernández A, Guimarães PR, Holland JN (2012) Abiotic factors shape temporal variation in the structure of an ant-plant network. Arthropod Plant Interact 6:289–295

    Article  Google Scholar 

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

    Google Scholar 

  • Ronquist F, Liljeblad J (2001) Evolution of the gall wasp–host plant association. Evolution 55:2503–2522

    CAS  PubMed  Google Scholar 

  • Ronquist F, Nieves-Aldrey JL, Buffington ML, Liu Z, Liljeblad J, Nylander JAA (2015) Phylogeny, evolution and classification of gall wasps: The plot thickens. PLoS ONE 10:e0123301

    Article  PubMed  PubMed Central  Google Scholar 

  • Schädler M, Brandl R, Kempel A (2010) Host plant genotype determines bottom-up effects in an aphid-parasitoid-predator system. Entomol Exp Appl 135:162–169

    Article  Google Scholar 

  • Schönrogge K, Crawley MJ (2000) Quantitative webs as a means of assessing the impact of alien insects. J Anim Ecol 69:841–868

    Article  PubMed  Google Scholar 

  • Schönrogge K, Moriya S, Melika G, Randle Z, Begg T, Aebi A, Stone GN (2006) Early parasitoid recruitment in invading cynipid galls. Galling arthropods and their associates. Springer, Tokyo, pp 91–101

    Chapter  Google Scholar 

  • Sebastian-Gonzalez E, Dalsgaard B, Sandel B, Guimaraes PR (2015) Macroecological trends in nestedness and modularity of seed-dispersal networks: human impact matters. Global Ecol Biogeogr 24:293–303

    Article  Google Scholar 

  • Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Ann Rev Plant Biol 60:561–588

    Article  CAS  Google Scholar 

  • Staab M, Fornoff F, Klein AM, Blüthgen N (2017) Ants at plant wounds: a little-known trophic interaction with evolutionary implications for ant-plant interactions. Am Nat 190:442–450

    Article  PubMed  Google Scholar 

  • Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tovar-Sánchez E, Oyama K (2006) Effect of hybridization of the Quercus crassifolia x Quercus crassipes complex on the community structure of endophagous insects. Oecologia 147:702–713

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol Syst 48:25–48

    Article  Google Scholar 

  • Underwood EC, Viers JH, Klausmeyer KR, Cox RL, Shaw MR (2009) Threats and biodiversity in the mediterranean biome. Divers Distrib 15:188–197

    Article  Google Scholar 

  • Valencia AS (2004) Diversidad del género Quercus (Fagaceae) en México. Bot Sci 75:33–53

    Google Scholar 

  • Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Welti EAR, Joern A (2015) Structure of trophic and mutualistic networks across broad environmental gradients. Ecol Evol 5:326–334

    Article  PubMed  Google Scholar 

  • Whitham TG, Martinsen GD, Floate KD, Dungey HS, 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 

  • Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    Article  CAS  PubMed  Google Scholar 

  • Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM, Keith AR, Smith DS (2012) Community specificity: life and afterlife effects of genes. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2012.01.005

    Article  PubMed  Google Scholar 

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Acknowledgements

The study was funded by Coordination of Scientific Research (UMSNH) project 005. This project was supported by CONACYT Project CB105755 and CONACYT PDC2016-Project-3053.

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YML, KO, and PCR: planned and designed the research. GPL MAZ, and PCR: conducted fieldwork. AGR, GPL, and KO: performed laboratory work. YML, WSA, MF, CDC, KSE, MAZ: conducted analyzed data. YML, WSA, AGR, KO, MF, KSE, MAZ, and PCR: The first draft of the manuscript was written. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Pablo Cuevas-Reyes.

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Maldonado-López, Y., de Araújo, W.S., González-Rodríguez, A. et al. Quantitative trophic networks of insect gallers and their parasitoids in the hybrid oak complex Quercus magnoliifolia x Quercus resinosa. Arthropod-Plant Interactions 16, 631–643 (2022). https://doi.org/10.1007/s11829-022-09927-8

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