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  • Print publication year: 2011
  • Online publication date: January 2012

4 - Fig–fig wasp mutualism: the fall of the strict cospeciation paradigm?

Summary

Introduction

At least three classic systems of nursery pollination mutualism are known: the fig (Ficus, Moraceae) – agaonid (Hymenoptera, Chalcidoidea) association (Cook and Rasplus 2003), the yucca (Yucca, Hesperoyucca; Agavaceae) – yucca moths (Tegeticula, Parategeticula; Lepidoptera, Prodoxidae) association (Pellmyr 2003) and the Glodichion (Phyllanthaceae) – Epicephala moths (Lepidoptera, Gracillariidae) association (Kato et al. 2003). All these mutualisms are obligate, which means that each partner depends on the other for its own reproductive success. The insect pollinates the flowers and oviposits in the plant ovaries where the insect larvae subsequently feed on a subset of the developing seeds. A shift from mutualism to parasitism by the pollinating insect would lead to reproduction failure of the plant and, without host shift, to the extinction of both lineages. Therefore, the speciation of mutualistic pollinators is generally believed to be driven by the speciation of their host-plants. In this hypothesis, when an ancestral plant species splits into two daughter species, its mutualistic pollinator also splits. This scenario should result in perfect congruence of hosts and pollinator phylogenies (Farenholz’s rule) (Farenholz 1913). However, this seems increasingly unlikely. Indeed, more and more studies on different coevolved associations show that a strict Farenholz’s rule is not respected, even when a high level of host specificity exists (e.g. Paterson and Banks 2001; Desdevises et al. 2002; Charleston and Perkins 2006).

Topological incongruence between host and associate phylogenetic trees can result from processes like host switching, sorting events (extinction and lineage sorting), duplication events (speciation of the parasite independent of the host), and failure of the associate to diverge when the host diverges (“missing the boat”) (Page 1991; Page 1994; Page and Charleston 1998; Legendre et al. 2002; Charleston and Perkins 2006).

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References
Akaike, H. 1973 Second International Symposium on Information TheoryBudapest, HungaryAkad. Kiado
Berg, C. C.Corner, E. J. H. 2005
Borges, R. M.Bessiere, J. M.Hossaert-McKey, M. 2008 The chemical ecology of seed dispersal in monoecious and dioecious figsFunctional Ecology 22 484
Charleston, M. A. 1998 Jungles: a new solution to the host/parasite phylogeny reconciliation problemMathematical Biosciences 149 191
Charleston, M. A.Page, R. D. M. 2002
Charleston, M. A.Perkins, S. L. 2006 Traversing the tangle: algorithms and applications for cophylogenetic studiesJournal of Biomedical Informatics 39 62
Compton, S. G.Holton, K. C.Rashbrook, V. K.Noort, S. v.Vincent, S. L.Ware, A.B. 1991 Studies of a non-pollinating agaonid fig waspBiotropica 23 188
Conow, C.Fielder, D.Ovadia, Y.Libeskind-Hadas, R. 2010 Jane: a new tool for the cophylogeny reconstruction problemAlgorithms for Molecular Biology 5 16
Cook, J. M.Rasplus, J.-Y. 2003 Mutualists with attitude: coevolving fig wasps and figsTrends in Ecology and Evolution 18 241
Cook, J. M.Segar, S. T. 2010 Speciation in fig waspsEcological Entomology 35 54
Cook, J. M.Bean, D.Power, S. A.Dixon, D. J. 2004 Evolution of a complex coevolved trait: active pollination in a genus of fig waspsJournal of Evolutionary Biology 17 238
Corner, E. J. H. 1958 An introduction to the distribution of FicusReinwardtia 4 325
Cruaud, A.Jabbour-Zahab, R.Genson, G.Cruaud, C.Couloux, A.Kjellberg, F.van Noort, S.Rasplus, J.-Y. 2010 Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approachCladistics 26 359
Cruaud, A.Jabbour-Zahab, R.Genson, G.Couloux, A.Yan-Qiong, P.Da Rong, Y.Ubaidillah, R.Pereira, R. A. S.Kjellberg, F.Van Noort, S.Kerdelhué, C.Rasplus, J.-Y. 2011 Out-of-Australia and back again: the worldwide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae)Journal of Biogeography, Special Paper
Desdevises, Y.Morand, S.Jousson, O.Legendre, P. 2002 Coevolution between lamellodiscus (monogenea:diplectanidae) and sapridae (Telestostei): the study of a complex host–parasite systemEvolution 56 2459
Drummond, A. J.Ashton, B.Cheung, M.Heled, J.Kearse, M.Moir, R.Stones-Havas, S.Thierer, T.Wilson, A. 2007 http://www.geneious.com/
Erasmus, C.van Noort, S.Jousselin, E.Greef, J. 2007 Molecular phylogeny of fig wasps pollinators (Agaonidae, Hymenoptera) of Ficus section GaloglychiaZoologica Scripta 36 61
Erixon, P.Svennblad, B.Britton, T.Oxelman, B. 2003 Reliability of bayesian posterior probabilities and bootstrap frequencies in phylogeneticsSystematic Biology 52 665
Farenholz, H. 1913 Ectoparasiten und AbstammungslehreZoologische Anzeiger 41 371
Felsenstein, J.Kishino, H. 1993 Is there something wrong with the bootstrap on phylogenies? A reply to Hillis and BullSystematic Biology 42 193
Gillespie, J. J.Cannone, J. J.Gutell, R. R.Cognato, A. 2004 A secondary structural model of the 28S rRNA expansion segments D2 and D3 from rootworms and related leaf beetles (Coleoptera : Chrysomelidae; Galerucinae)Insect Molecular Biology 13 495
Gillespie, J. J.Johnston, J. S.Cannone, J. J.Gutell, R. R. 2006 Characteristics of the nuclear (18S, 5.8S, 28S and 5S) and mitochondrial (12S and 16S) rRNA genes of (Insecta: Hymenoptera): structure, organization and retrotransposable elementsInsect Molecular Biology 15 657
Gillespie, J. J.Munro, J. B.Heraty, J. M.Yoder, M. J.Owen, A. K.Carmichael, A.E. 2005 A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera : Chalcidoidea)Molecular Biology and Evolution 22 1593
Haine, E. R.Martin, J.Cook, J. M. 2006 Deep mtDNA divergences indicate cryptic species in a fig-pollinating waspBMC Evolutionary Biology 6 83
Herre, E. A.Machado, C. A.Bermingham, E.Nason, J. D.Windsor, D. M.McCafferty, S.Van Houten, W.Bachmann, K. 1996 Molecular phylogenies of figs and their pollinator waspsJournal of Biogeography 23 521
Hossaert-McKey, M.Giberneau, M.Frey, J. E. 1994 Chemosensory attraction of fig wasps to substances produced by receptive figsEntomologia Experientia et Applicata 70 185
Huelsenbeck, J. P.Ronquist, F. 2001 MrBayes: Bayesian inferences of phylogenyBioinformatics 17 754
Huelsenbeck, J. P.Larget, B.Miller, R. E.Ronquist, F. 2002 Potential applications and pitfalls of Bayesian inference in phylogenySystematic Biology 51 673
Jackson, A. P. 2004 Cophylogeny of the Ficus microcosmBiological Reviews 79 751
Jackson, A. P.Machado, C. A.Robbins, N.Herre, E. A. 2008 Multi-locus phylogenetic analysis of neotropical figs does not support cospeciation with the pollinators: The importance of systematic scale in fig.wasp cophylogenetic studiesSymbiosis 45 57
Jiang, Z. F.Huang, D. W.Zhu, C. D.Zhen, W. Q. 2006 New insights into the phylogeny of fig pollinators using Bayesian analysesMolecular Phylogenetics and Evolution 38 306
Jousselin, E.Kjellberg, F. 2001 The functional implications of active and passive pollination in dioecious figsEcology Letters 4 151
Jousselin, E.Rasplus, J. Y.Kjellberg, F. 2003 Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Evolution 57
Jousselin, E.Desdevises, Y.Coeur d’Acier, A. 2009 Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphidsProceedings of the Royal Society B 276 187
Jousselin, E.van Noort, S.Rasplus, J. Y.Rønsted, N.Erasmus, C.Greeff, J. 2008 One tree to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig waspsEvolution 62 1777
Kato, M.Takimura, A.Kawakita, A. 2003 An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae)Proceedings of the National Acacemy of Sciences USA 100 5264
Kawakita, A.Takimura, A.Terachi, T.Sota, T.Kato, M. 2004 Cospeciation analysis of an obligate pollination mutualism: Have Glochidion trees (Euphorbiaceae) and pollinating Epicephala moths (Gracillariidae) diversified in parallel?Evolution 58 2201
Kerdelhué, C.Hochberg, M.Rasplus, J. Y. 1997 Active pollination of Ficus sur by two sympatric fig wasp species in West AfricaBiotropica 29 69
Kjellberg, F.Jousselin, E.Hossaert-McKey, M.Rasplus, J. Y. 2005 Biology, Ecology, and Evolution of Gall-Inducing ArthropodsRaman, A.Schaefer, C. W.Withers, T. M.Enfield, NHSciences Publishers, Inc.
Kjer, K. M. 1995 Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogsMolecular Phylogenetics and Evolution 4 314
Legendre, P.Desdevises, Y.Bazin, E. 2002 A statistical test for host–parasite coevolutionSystematic Biology 51 217
Light, J. E.Hafner, M. S. 2008 Codivergence in heteromyid rodents (Rodentia:Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera:Anoplura)Systematic Biology 57 449
Lopez-Vaamonde, C.Dixon, D. J.Cook, J.Rasplus, J. Y. 2002 Revision of the Australian species of Pleistodontes (Hymenoptera:Agaonidae) fig-pollinating wasps and their host plant associationsZoological Journal of the Linnean Society 136 637
Lopez-Vaamonde, C.Rasplus, J. Y.Weiblen, G. D.Cook, J. M. 2001 Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasitesMolecular Phylogenetics and Evolution 21 55
Lopez-Vaamonde, C.Cook, J. M.Rasplus, J.-Y.Machado, C. A.Weiblen, G. 2009 Molecular dating and biogeography of fig-pollinating waspsMolecular Phylogenetics and Evolution 52 715
Machado, C. A.Robbins, N.Gilbert, M. T. P.Herre, E. A. 2005 Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualismProceedings of the National Academy of Sciences USA 102 6558
Machado, C. A.Jousselin, E.Kjellberg, F.Compton, S.Herre, E. A. 2001 Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating waspsProceedings of the Royal Society of London B 268 685
Marshall, D. C.Simon, C.Buckley, T. R. 2006 Accurate branch length estimation in partitioned Bayesian analyses requires accommodation of among-partition rate variation and attention to branch length priorsSystematic Biology 55 993
Marussich, W. A.Machado, C. A. 2007 Host-specificity and coevolution among pollinating and non-pollinating New World fig waspsMolecular Ecology 16 1925
McGuire, J. A.Witt, C. C.Altshuler, D. L.Remsen, J. V. J. 2007 Phylogenetic systematics and biogeography of hummingbirds: bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategySystematic Biology 56 837
Meier-Kolthoff, J. P.Auch, A. F.Huson, D. H.Goker, M. 2007 CopyCat: cophylogenetic analysis toolBioinformatics 23 898
Michaloud, G.Michaloud-Pelletier, S.Wiebes, J. T.Berg, C. C. 1985 The co-occurrence of two pollinating species of fig wasp on one species of figProceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, (C) 88 93
Molbo, D.Machado, C. A.Sevenster, J. G.Keller, L.Herre, E. A. 2003 Cryptic species of fig-pollinating wasps: implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptationProceedings of the National Academy of Sciences USA 100 5867
Nylander, J. A. A. 2004
Nylander, J. A. A.Ronquist, F.Huelsenbeck, J. P.Nieves-Aldrey, J. L. 2004 Bayesian phylogenetic analysis of combined dataSystematic Biology 53 47
Nylander, J. A. A.Wilgenbusch, J. C.Warren, D. L.Swofford, D. L. 2008 AWTY (are we there yet?): a system for grafical exploration of MCMC convergence in Bayesian phylogeneticsBioinformatics 24 581
Page, R. D. M. 1991 Clocks, clades, and cospeciation: comparing rates of evolution and timing of cospeciationn events in host-parasite assemblagesSystematic Zoology 40 188
Page, R. D. M. 1994 Parallel phylogenies – reconstructing the history of host-parasite assemblagesCladistics 10 155
Page, R. D. M.Charleston, M. A. 1998 Trees within trees: phylogeny and historical associationsTrends in Ecology and Evolution 13 356
Paterson, A. M.Banks, J. B. 2001 Analytical approaches to measuring cospeciation of host and parasites: through a glass, darklyInternational Journal of Parasitology 31 1012
Pellmyr, O. 2003 Yuccas, yucca moths, and coevolution: a reviewAnnals of the Missouri Botanical Garden 90 35
Peng, Y. Q.Duan, Z.-B.Yang, D. R.Rasplus, J. Y. 2008 Co-occurrence of two Eupristina species on Ficus altissima in Xishuangbanna, SW ChinaSymbiosis 45 9
Percy, D. M.Page, R. D. M.Cronk, Q. C. B. 2004 Plant–insect interactions: double-dating associated insect and plant lineages reveals asynchronous radiationsSystematic Biology 53 120
Rambaut, A.Drummond, A. J. 2003 http://tree.bio.ed.ac.uk/software/tracer/
Ramirez, W.B. 1974 Coevolution of and AgaonidaeAnnals of the Missouri Botanical Garden 61 770
Ramirez, W. B. 1991 Evolution of the mandibular appendage in fig wasps (Hymenoptera: Agaonidae)Revista de Biologia Tropical 39 87
Rasplus, J. Y. 1996 The Biodiversity of African PlantsMaesen, L. J. G. Van DerBurgt, X. M. Van DerRooy, J. M. Van Medenbach DeWageningen, The NetherlandsKluwer Academic Publishers
Renoult, J. P.Kjellberg, F.Grout, C.Santoni, S.Khadari, B. 2009 Cyto-nuclear discordance in the phylogeny of section and host shifts in plant–pollinator associationsBMC Evolutionary Biology 9 248
Rønsted, N.Salvo, G.Savolainen, V. 2007 Biogeographical and phylogenetic origins of African fig species (Ficus section Galoglychia)Molecular Phylogenetics and Evolution 43 190
Rønsted, N.Weiblen, G.Savolainen, V.Cook, J. 2008 Phylogeny, biogeography, and ecology of Ficus section Malvanthera (Moraceae)Molecular Phylogenetics and Evolution 48 12
Rønsted, N.Weiblen, G.Clement, W. L.Zerega, N. J. C.Savolainen, V. 2008 Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualismSymbiosis 45 45
Rønsted, N.Weiblen, G. D.Cook, J. M.Salamin, N.Machado, C. A.Savolainen, P. 2005 60 million years of codivergence in the fig-wasp symbiosisProceedings of the Royal Society B: Biological Sciences 272 2593
Shanahan, M.So, S.Compton, S.Corlett, R. 2001 Fig-eating by vertebrate frugivores: a global reviewBiological Reviews of the Cambridge Philosophical Society 76 529
Silvieus, S. I.Clement, W. L.Weiblen, G. D. 2007 Specialization, Speciation, and Radiation: the Evolutionary Biology of Herbivorous InsectsBerkeley, CAUniversity of California Press
Simmons, M. P.Pickett, K. M.Miya, M. 2004 How meaningful are Bayesian support values?Molecular Biology and Evolution 21 188
Smith, C. I.Pellmyr, O.Althoff, D. M.Balcazar-Lara, M.Leebens-Mack, J.Segraves, K. A. 2008 Pattern and timing of diversification in Yucca (Agavaceae): specialized pollination does not escalate rates of diversificationProceedings of the Royal Society 275 249
Stamatakis, A. 2006
Stamatakis, A. 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed modelsBioinformatics 22 2688
Su, Z. H.Iino, H.Nakamura, K.Serrato, A.Oyama, K. 2008 Breakdown of the one-to-one rule in Mexican fig-wasp associations inferred by molecular phylogenetic analysisSymbiosis 45 73
Tamura, K.Dudley, J.Nei, M.Kumar, S. 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0Molecular Biology and Evolution 24 1596
Thompson, J. D.Higgins, D. G.Gibson, J. T. 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignement through sequence weighting, position specific gap penalties and weight matrix choiceNucleic Acids Research 22 4673
Weiblen, G. D. 2000 Phylogenetic relationships of functionally dioecious Ficus (Moraceae) based on ribosomal DNA sequences and morphologyAmerican Journal of Botany 87 1342
Weiblen, G. D. 2001 Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphologySystematic Biology 50 243
Weiblen, G. D. 2002 How to be a fig wasp?Annual Review of Entomology 47 299
Weiblen, G. D. 2004 Correlated evolution in fig pollinationSystematic Biology 53 128
Weiblen, G. D.Bush, G. L. 2002 Speciation in fig pollinators and parasitesMolecular Ecology 11 1573
Wiebes, J. T. 1982 The phylogeny of the Agaonidae (Hymenoptera, Chalcidoidea)Netherlands Journal of Zoology 32 395
Wiens, J. J.Fetzner, J. W.Parkinson, C. L.Reeder, T. W. 2005 Hylid frog phylogeny and sampling strategies for speciose cladesSystematic Biology 54 719
Yokohama, J. 1994 Molecular phylogeny and coevolutionPlant Species Biology 9 163