An extreme case of plant-insect codiversification: figs and fig-pollinating wasps

Astrid Cruaud; Nina Rønsted; Bhanumas Chanterasuwan; Lien Siang Chou; Wendy L. Clement; Arnaud Couloux; Benjamin Cousins; Gwenaëlle 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 Schramm; Rosichon Ubaidillah; Simon van Noort; George D. Weiblen; Da-Rong Yang; Anak Yodpinyanee; Ran Libeskind-Hadas; James M. Cook; Jean-Yves Rasplus; Vincent Savolainen

doi:10.1093/sysbio/sys068

An extreme case of plant-insect codiversification: figs and fig-pollinating wasps

Astrid Cruaud, Nina Rønsted, Bhanumas Chanterasuwan, Lien Siang Chou, Wendy L. Clement, Arnaud Couloux, Benjamin Cousins, Gwenaëlle 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

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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 language	English
Journal	Systematic Biology
Volume	61
Issue number	6
Pages (from-to)	1029-1047
Number of pages	19
ISSN	1063-5157
DOIs	https://doi.org/10.1093/sysbio/sys068
Publication status	Published - Dec 2012

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Cruaud, A., Rønsted, N., Chanterasuwan, B., Chou, L. S., Clement, W. L., Couloux, A., Cousins, B., Genson, G., Harrison, R. D., Hanson, P. E., Hossaert-McKey, M., Jabbour-Zahab, R., Jousselin, E., Kerdelhué, C., Kjellberg, F., Lopez-Vaamonde, C., Peebles, J., Peng, Y-Q., Pereira, R. A. S., ... Savolainen, V. (2012). An extreme case of plant-insect codiversification: figs and fig-pollinating wasps. Systematic Biology, 61(6), 1029-1047. https://doi.org/10.1093/sysbio/sys068

Cruaud, A, Rønsted, N, Chanterasuwan, B, Chou, LS, Clement, WL, Couloux, A, Cousins, B, Genson, G, Harrison, RD, Hanson, PE, Hossaert-McKey, M, Jabbour-Zahab, R, Jousselin, E, Kerdelhué, C, Kjellberg, F, Lopez-Vaamonde, C, Peebles, J, Peng, Y-Q, Pereira, RAS, Schramm, T, Ubaidillah, R, van Noort, S, Weiblen, GD, Yang, D-R, Yodpinyanee, A, Libeskind-Hadas, R, Cook, JM, Rasplus, J-Y & Savolainen, V 2012, 'An extreme case of plant-insect codiversification: figs and fig-pollinating wasps', Systematic Biology, vol. 61, no. 6, pp. 1029-1047. https://doi.org/10.1093/sysbio/sys068

@article{3f7cf016f2e64afa87b679a57e1bad13,

title = "An extreme case of plant-insect codiversification: figs and fig-pollinating wasps",

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.]",

author = "Astrid Cruaud and Nina R{\o}nsted and Bhanumas Chanterasuwan and Chou, {Lien Siang} and Clement, {Wendy L.} and Arnaud Couloux and Benjamin Cousins and Gwena{\"e}lle Genson and Harrison, {Rhett D.} and Hanson, {Paul E.} and Martine Hossaert-McKey and Roula Jabbour-Zahab and Emmanuelle Jousselin and Carole Kerdelhu{\'e} and Finn Kjellberg and Carlos Lopez-Vaamonde and John Peebles and Yan-Qiong Peng and Pereira, {Rodrigo Augusto Santinelo} and Tselil Schramm and Rosichon Ubaidillah and {van Noort}, Simon and Weiblen, {George D.} and Da-Rong Yang and Anak Yodpinyanee and Ran Libeskind-Hadas and Cook, {James M.} and Jean-Yves Rasplus and Vincent Savolainen",

year = "2012",

month = dec,

doi = "10.1093/sysbio/sys068",

language = "English",

volume = "61",

pages = "1029--1047",

journal = "Systematic Biology",

issn = "1063-5157",

publisher = "Oxford University Press",

number = "6",

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TY - JOUR

T1 - An extreme case of plant-insect codiversification

T2 - figs and fig-pollinating wasps

AU - Cruaud, Astrid

AU - Rønsted, Nina

AU - Chanterasuwan, Bhanumas

AU - Chou, Lien Siang

AU - Clement, Wendy L.

AU - Couloux, Arnaud

AU - Cousins, Benjamin

AU - Genson, Gwenaëlle

AU - Harrison, Rhett D.

AU - Hanson, Paul E.

AU - Hossaert-McKey, Martine

AU - Jabbour-Zahab, Roula

AU - Jousselin, Emmanuelle

AU - Kerdelhué, Carole

AU - Kjellberg, Finn

AU - Lopez-Vaamonde, Carlos

AU - Peebles, John

AU - Peng, Yan-Qiong

AU - Pereira, Rodrigo Augusto Santinelo

AU - Schramm, Tselil

AU - Ubaidillah, Rosichon

AU - van Noort, Simon

AU - Weiblen, George D.

AU - Yang, Da-Rong

AU - Yodpinyanee, Anak

AU - Libeskind-Hadas, Ran

AU - Cook, James M.

AU - Rasplus, Jean-Yves

AU - Savolainen, Vincent

PY - 2012/12

Y1 - 2012/12

N2 - 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.]

AB - 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.]

U2 - 10.1093/sysbio/sys068

DO - 10.1093/sysbio/sys068

M3 - Journal article

C2 - 22848088

SN - 1063-5157

VL - 61

SP - 1029

EP - 1047

JO - Systematic Biology

JF - Systematic Biology

IS - 6

ER -

An extreme case of plant-insect codiversification: figs and fig-pollinating wasps

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