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Geographic structuring into vicariant species-pairs in a wide-ranging, high-dispersal plant–insect mutualism: the case of Ficus racemosa and its pollinating wasps

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Abstract

Ficus and their mutualistic pollinating wasps provide a unique model to investigate joint diversification in a high dispersal system. We investigate genetic structuring in an extremely wide-ranging Ficus species, Ficus racemosa, and its pollinating wasp throughout their range, which extends from India to Australia. Our samples were structured into four large, vicariant populations of figs and wasps which may correspond to distinct (sub)species, located in India, China-Thailand, Borneo, and Australia. However, the genetically most divergent group was the Indian population for the figs and the China-Thailand population for the wasps, suggesting different evolutionary histories of populations. Molecular dating for the wasps shows that diversification of the pollinator clade is surprisingly old, beginning about 13.6 Ma. Data on both the host fig species and its pollinating wasps suggest that strong genetic flow within biogeographic groups over several hundreds of kilometers has limited genetic and morphological differentiation and, potentially, local adaptation. This is probably due to long-distance dispersal of pollinating wasps. The genetic clustering into large geographic units observed in F. racemosa and its pollinators is reminiscent of what can be observed in some other high-dispersal organisms characterized by morphology that varies little over huge distances. The implications of strong gene flow for diversification processes and adaptation to different ecological conditions in Ficus and their pollinating wasps are just beginning to emerge.

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References

  • Ahmed S, Dawson DA, Compton SG et al (2007) Characterization of microsatellite loci in the African fig Ficus sycomorus L. (Moraceae). Mol Ecol Notes 7:1175–1177

    Article  CAS  Google Scholar 

  • Ahmed S, Compton SG, Butlin RK et al (2009) Wind-borne insects mediate directional pollen transfer between desert fig trees 160 kilometers apart. Proc Natl Acad Sci USA 106:20342–20347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov PN, Csaki F (eds) Second international symposium on information theory. Akad, Kiado, pp 267–281

    Google Scholar 

  • Alvarez N, McKey D, Kjellberg F et al (2010) Phylogeography and historical biogeography of obligate specific mutualisms. In: Morand S, Krasnov BR (eds) The biogeography of host-parasite interactions. Oxford University Press, Oxford, p 277

    Google Scholar 

  • Ashley MV (2010) Plant parentage, pollination, and dispersal: how DNA microsatellites have altered the landscape. Crit Rev Plant Sci 29:148–161

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 57:289–300

    Google Scholar 

  • Berg CC, Corner EJH (2005) Moraceae (Ficus). In: Nooteboom HP (ed) Flora Malesiana. National Herbarium Nederland, Leiden

    Google Scholar 

  • Borges RM (2015) How to be a fig wasp parasite on the fig–fig wasp mutualism. Curr Opin Insect Sci 8:34–40

    Article  Google Scholar 

  • Buschbom J, Yanbaev Y, Degen B (2011) Efficient long-distance gene flow into an isolated relict oak stand. J Hered 22:484–493

    Google Scholar 

  • Chen Y, Compton SG, Liu M et al (2012) Fig trees at the northern limit of their range: the distributions of cryptic pollinators indicate multiple glacial refugia. Mol Ecol 21:1687–1701

    Article  PubMed  Google Scholar 

  • Conchou L, Cabioch L, Rodriguez LJV et al (2014) Daily rhythm of mutualistic pollinator activity and scent emission in Ficus septica: ecological differentiation between co-occurring pollinators and potential consequences for chemical communication and facilitation of host speciation. PLoS ONE 9:e103581

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornille A, Underhill JG, Cruaud A et al (2012) Floral volatiles, pollinator sharing and diversification in the fig–wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proc R Soc B 279:1731–1739

    Article  CAS  PubMed  Google Scholar 

  • Cruaud A, Jabbour-Zahab R, Genson G et al (2010) Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approach. Cladistics 26:359–387

    Google Scholar 

  • Cruaud A, Jabbour-Zahab R, Genson G et al (2011) Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea). BMC Evol Biol 11:178–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Cruaud A, Rønsted N, Chantarasuwan B et al (2012) An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps. Syst Biol 61:1029–1047

    Article  PubMed  PubMed Central  Google Scholar 

  • Cunha RL, Blanc F, Bonhomme F et al (2011) Evolutionary patterns in pearl oysters of the genus Pinctada (Bivalvia: Pteriidae). Mar Biotechnol 13:181–192

    Article  CAS  PubMed  Google Scholar 

  • Darwell CT, Al-Beidh S, Cook JM (2014) Molecular species delimitation of a symbiotic fig-pollinating wasp species complex reveals extreme deviation from reciprocal partner specificity. BMC Evol Biol 14:189

    Article  PubMed  PubMed Central  Google Scholar 

  • Dev SA, Kjellberg F, Hossaert-McKey M et al (2011) Fine-scale population genetic structure of two dioecious Indian keystone species, Ficus hispida and Ficus exasperata (Moraceae). Biotropica 43:309–316

    Article  Google Scholar 

  • Dick CW, Lewis SL, Maslin M et al (2013) Neogene origins and implied warmth tolerance of Amazon tree species. Ecol Evol 3:162–169

    Article  PubMed Central  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–221

    Article  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Gu X (1995) Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol Biol Evol 12:546–557

    CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H et al (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison RD (2005) Figs and the diversity of tropical rainforests. Bioscience 55:1053–1064

    Article  Google Scholar 

  • Harrison RD, Rasplus J-Y (2006) Dispersal of fig pollinators in Asian tropical rain forests. J Trop Ecol 22:631–639

    Article  Google Scholar 

  • Heer K, Kalko EKV, Albrecht L, Garcia-Villacorta R, Staeps FC, Herre EA, Dick CW (2015) Spatial scales of genetic structure in free-standing and strangler figs (Ficus, Moraceae) inhabiting Neotropical forests. PLoS ONE 10:e0133581

    Article  PubMed  PubMed Central  Google Scholar 

  • Heinrichs J, Hentschel J, Feldberg K et al (2009) Phylogenetic biogeography and taxonomy of disjunctly distributed bryophytes. J Syst Evol 47:497–508

    Article  Google Scholar 

  • Heinze B (2007) A database of PCR primers for the chloroplast genomes of higher plants. Plant Methods 3:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopkins MJ (2011) How species longevity, intraspecific morphological variation, and geographic range size are related: a comparison using late Cambrian trilobites. Evolution 65:3253–3273

    Article  PubMed  Google Scholar 

  • Hossaert-McKey M, Soler C, Schatz B et al (2010) Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20:75–88

    Article  Google Scholar 

  • Jablonski D, Roy K (2003) Geographical range and speciation in fossil and living mollusks. Proc R Soc B 270:401–406

    Article  PubMed  PubMed Central  Google Scholar 

  • Jevanandam N, Goh AGR, Corlett RT (2013) Climate warming and the potential 16 extinction of fig wasps, the obligate pollinators of figs. Biol Lett 9:20130041

    Article  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Kuma K, Toh H et al (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khadari B, Hochu I, Santoni S et al (2001) Identification and characterization of microsatellite loci in the common fig (Ficus carica L.) and representative species of the genus Ficus. Mol Ecol Notes 1:191–193

    Article  CAS  Google Scholar 

  • Kinland BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

    Article  Google Scholar 

  • Kjellberg F, Proffit M (2016) Tracking the elusive history of diversification in plant-herbivorous insect-parasitoid food webs: insights from figs and fig-wasps. Mol Ecol 25:843–845

    Article  PubMed  Google Scholar 

  • Kjellberg F, Jousselin E, Hossaert-McKey M et al (2005) Biology, ecology, and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In: Raman A, Schaefer W, Withers TM (eds) Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc, Enfield (NH) USA, Plymouth, pp 539–572

    Google Scholar 

  • Kobmoo N, Hossaert-McKey M, Rasplus J-Y et al (2010) Ficus racemosa is pollinated by a single population of a single agaonid wasp species in continental South-East Asia. Mol Ecol 19:2700–2712

    Article  CAS  PubMed  Google Scholar 

  • Kremer A, Ronce O, Robledo-Arnuncio JJ et al (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15:378–392

    Article  PubMed  PubMed Central  Google Scholar 

  • Krishnan A, Ghara M, Kasinathan S et al (2015) Plant reproductive traits mediate tritrophic feedback effects within an obligate brood-site pollination mutualism. Oecologia 179:797–809

    Article  PubMed  Google Scholar 

  • Léotard G, Debout G, Dalecky A et al (2009) Range expansion drives dispersal evolution in an equatorial three-species symbiosis. PLoS ONE 4:e5377

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis LR, Rozzi R, Goffinet B (2014) Direct long-distance dispersal shapes a New World amphitropical disjunction in the dispersal-limited dung moss Tetraplodon (Bryopsida: Splachnaceae). J Biogeogr 41:2385–2395

    Article  Google Scholar 

  • Lin S-Y, Chou L-S, Di Giusto B et al (2015) Sexual specialization in phenology in dioecious Ficus benguetensis and its consequences for the mutualism. Bot stud 56:32

    Article  Google Scholar 

  • Liu M, Zhao R, Chen Y et al (2014) Competitive exclusion among fig wasps achieved via entrainment of host plant flowering phenology. PLoS ONE 9:e97783

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu M, Compton SG, Peng F-E et al (2015) Movements of genes between populations: are pollinators more effective at transferring their own or plant genetic markers? Proc R Soc B 282:20150290

    Article  PubMed  PubMed Central  Google Scholar 

  • Loiselle BA, Sork VL, Nason J et al (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Moe AM, Weiblen GD (2010) Molecular divergence in allopatric Ceratosolen (Agaonidae) pollinators of geographically widespread Ficus (Moraceae) species. Ann Entomol Soc Am 103:1025–1037

    Article  Google Scholar 

  • Moe AM, Weiblen GD (2011) Development and characterization of microsatellite loci in dioecious figs (Ficus, Moraceae). Am J Bot Notes Prot 98:e25–e27

    Article  CAS  Google Scholar 

  • Nunes FLD, Norris RD, Knowlton N (2011) Long distance dispersal and connectivity in amphi-atlantic corals at regional and basin scales. PLoS ONE 6:e22298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nylander JAA (2004) MrAIC.pl. In: Nylander JAA (ed) Evolutionary Biology Centre. Uppsala University, Uppsala

    Google Scholar 

  • Oleksy R, Racey PA, Jones G (2015) High-resolution GPS tracking reveals habitat selection and the potential for long-distance seed dispersal by Madagascan flying foxes Pteropus rufus. Glob Ecol Conserv 3:678–692

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Ann Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/darwin

  • Pokorny L, Oliván G, Shaw AJ (2011) Phylogeographic patterns in two Southern Hemisphere species of Calyptrochaeta (Daltoniaceae, Bryophyta). Syst Bot 36:542–553

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A (2006) FigTree. http://tree.bio.ed.ac.uk/software/figtree/

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Renoult JP, Kjellberg F, Grout C et al (2009) Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evol Biol 9:248

    Article  PubMed  PubMed Central  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Shilton LA, Altringham JD, Compton SG et al (1999) Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc R Soc B 266:219–223

    Article  PubMed Central  Google Scholar 

  • Smith CI, Tank S, Godsoe W et al (2011) Comparative phylogeography of a coevolved community: concerted population expansions in Joshua trees and four yucca moths. PLoS ONE 6:e25628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soler C, Hossaert-McKey M, Buatois B et al (2011) Geographic variation of floral scent in a highly specialized pollination mutualism. Phytochemistry 72:74–81

    Article  CAS  PubMed  Google Scholar 

  • Sutton TL, Riegler M, Cook JM (2016) One step ahead: a parasitoid disperses farther and forms a wider geographic population than its fig wasp host. Mol Ecol 25:882–894

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Thompson AR, Thacker CE, Shaw EY (2005) Phylogeography of marine mutualists: parallel patterns of genetic structure between obligate goby and shrimp partners. Mol Ecol 14:3557–3572

    Article  CAS  PubMed  Google Scholar 

  • Tian E, Nason JD, Machado CA et al (2015) Lack of genetic isolation by distance, similar genetic structuring but different demographic histories in a fig-pollinating wasp mutualism. Mol Ecol 24:5976–5991

    Article  PubMed  Google Scholar 

  • Vignes H, Hossaert-McKey M, Beaune D et al (2006) Development and characterization of microsatellite markers for a monoecious Ficus species, Ficus insipida, and cross-species amplification among different sections of Ficus. Mol Ecol Notes 6:792–795

    Article  CAS  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  • Wang G, Cannon CH, Chen J (2016) Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa. Proc R Soc B 283:20152963

    Article  PubMed  Google Scholar 

  • Ware AB, Compton SG (1994) Dispersal of adult female fig wasps. 2. Movements between trees. Entomol Exp Appl 73:231–238

    Article  Google Scholar 

  • Yang L-Y, Machado CA, Dang X-D et al (2015) The incidence and pattern of copollinator diversification in dioecious and monoecious figs. Evolution 69:294–304

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu H, Nason JD (2013) Nuclear and chloroplast DNA phylogeography of Ficus hirta: obligate pollination mutualism and constraints on range expansion in response to climate change. New Phytol 197:276–289

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Song Q, Yang D (2006) Phenology of Ficus racemosa in Xishuangbanna, Southwest China. Biotropica 38:334–341

    Article  Google Scholar 

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Acknowledgments

This study was funded by the by the ANR Projects “nicefigs” (ANR-09-BLAN-0392-CSD 7; NSC 99-2923-B-002-001-MY3) and “biofigs” (ANR BDIV-006-001)/National Science Council, Taiwan, R. O. C. Led by M.H.M. We thank Marc Ancrenaz, James Cook, and Edmond Dounias for their help in collecting samples, and Doyle McKey for his useful comments on our paper. We are also grateful to the staff of the Center for Ecological Sciences, Bangalore and of Xishuangbanna Tropical Botanical Garden (XTBG, China) for their field assistance. Laboratory manipulations were done at CEFE (SMGE), CBGP and at the LABEX CEMEB facilities.

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Author notes

  1. M. H. Chevallier

    Present address: CIRAD, Station de Ligne-Paradi, Pôle de Protection des Plantes - 3Ps, 7 Chemin de l’irat, 97410, Saint-Pierre, La Réunion, France

  2. H. Vignes

    Present address: CIRAD UMR AGAP, 34398, Montpellier, France

  3. N. Kobmoo

    Present address: National Center for Genetic Engineering and Biotechnology (BIOTEC), 113 Thailand Science Park, Phahonyothin Road, Khlong Nueng, Khlong Luang, Pathum Thani, 12120, Thailand

Authors and Affiliations

  1. CEFE UMR 5175, CNRS, Université de Montpellier, Université Paul-Valéry Montpellier – EPHE, 1919 Route de Mende, 34293, Montpellier, Cedex 5, France

    A. Bain, M. H. Chevallier, H. Vignes, N. Kobmoo, F. Kjellberg & M. Hossaert-Mckey

  2. Institute of Ecology and Evolutionary Biology, College of Life Science, National Taiwan University, No. 1, Sec. 4, Roosevelt Rd., Taipei, 10617, Taiwan

    A. Bain

  3. Indian Institute of Science, Centre for Ecological Sciences, Bangalore, 560012, Karnataka, India

    R. M. Borges

  4. Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, China

    Y. Q. Peng

  5. INRA - UMR 1062 CBGP (INRA/IRD/CIRAD/supagro), 34988, Montferrier Sur Lez, France

    A. Cruaud & J. Y. Rasplus

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  1. A. Bain
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Correspondence to A. Bain.

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Bain, A., Borges, R.M., Chevallier, M.H. et al. Geographic structuring into vicariant species-pairs in a wide-ranging, high-dispersal plant–insect mutualism: the case of Ficus racemosa and its pollinating wasps. Evol Ecol 30, 663–684 (2016). https://doi.org/10.1007/s10682-016-9836-5

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