An Extreme case of plant-insect codiversification: Figs and fig-pollinating wasps

Astrid Cruaud, Nina Ronsted, Bhanumas Chantarasuwan, Lien Siang Chou, Wendy L. Clement, Arnaud Couloux, Benjamin Cousins, Gwenaélle Genson, Rhett D. Harrison, Paul E. Hanson, Martine Hossaert-Mckey, Roula Jabbour-Zahab, Emmanuelle Jousselin, Carole Kerdelhué, Finn Kjellberg, Carlos Lopez-Vaamonde, John Peebles, Yan Qiong Peng, Rodrigo Augusto Santinelo Pereira, Tselil SchrammRosichon Ubaidillah, Simon Van Noort, George D Weiblen, Da Rong Yang, Anak Yodpinyanee, Ran Libeskind-Hadas, James M. Cook, Jean Yves Rasplus, Vincent Savolainen

Research output: Contribution to journalArticlepeer-review

184 Scopus citations

Abstract

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant-insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by 750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77 of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study.We also developed a newanalytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, ather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.]

Original languageEnglish (US)
Pages (from-to)1029-1047
Number of pages19
JournalSystematic Biology
Volume61
Issue number6
DOIs
StatePublished - Dec 2012

Bibliographical note

Funding Information:
FUNDING This work was supported by the ANR projects “NiceFigs” and “BioFigs/National Science Council, Taiwan, R. O. C. code: 98WFA0100291” led by M.H.M. and L.S.C.; by a grant from the Carlsberg Foundation and a Marie Curie grant “CoEvol” to N.R.; grants from the Leverhulme Trust, NERC, the Royal Society, and the European Research Council to V.S.; NSC [project 99-2923-B-002-001-MY3 to L.S.C]; Fapesp [grant 04/10229-4 to R.A.S.P.]; NERC to J.M.C.; NSF [grant 0753306 Harvey Mudd College and R.L.H., B.C., J.P., and T.S] and the Howard Hughes Medical Institute [grant 52006301 to Harvey Mudd College and R.L.H., B.C., J.P., and T.S.]. Funding to pay the Open Access publication charges for this article was provided by The Natural History Museum of Denmark.

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