Biodiversity Science ›› 2018, Vol. 26 ›› Issue (3): 295-303.doi: 10.17520/biods.2017219

• Reviews • Previous Article     Next Article

Progress on the breakdown of one-to-one rule in symbiosis of figs and their pollinating wasps

Jianfeng Huang1#, Rui Xu2#, Yanqiong Peng1, *()   

  1. 1 Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303
    2 Yunnan Institute of Tropical Crops, Jinghong, Yunnan 666100
  • Received:2017-09-16 Accepted:2018-03-27 Online:2018-05-05
  • Peng Yanqiong
  • About author:

    # Co-first authors

The fig-fig-pollinating wasp symbiosis provides a model system for investigating the mutualistic interaction between plants and animals. A simple one-to-one rule was proposed to describe the highly specialized reciprocal relationships between figs and their species-specific pollinating fig wasps based on the initial studies: each fig tree species is obligatorily pollinated by one fig wasp species, and each wasp species can only reproduce in one fig species. With the deepening of research, however, increasing cases of breakdown in species-specificity have been reported, especially the reveal of cryptic pollinating fig wasp species progressively weaken the universality of one-to-one rule in fig-fig-pollinating wasp symbiosis. The documented cases of breakdown in the one-to-one rule were divided into two types, including copollinator and pollinator sharing, which have their own different mechanisms. Pollinator sharing is pollination of different species of Ficus by the same pollinator, while copollinator is the co-occurrence of more than one species of pollinators in one host fig. Here, the research progress on the breakdown of one-to-one rule is presented in three stages, i.e. morphological description, multidisciplinary evidence and discovery of cryptic pollinating wasp species. Some future challenges and research prospects resulted from the breakdown of one-to-one rule are outlined. Copollinators may lead to the interspecific hybridization between pollinator species, while pollinator sharing may result in the hybridization of host figs. Nonetheless, the hybridization in fig-fig-pollinating wasp symbiosis is very rare and suggests a strong level of reproductive isolation. Furthermore, the incidence and pattern of pollinator sharing and copollinator are differentiated in dioecious and monoecious figs, which suggests a differentiated host-specificity. The identification of cryptic species triggers the research of its speciation and co-occurrence, as well as the reassessment of pollinator biodiversity. Failing to recognize cryptic species also will limits the effectiveness of the controlled experiment in fig-fig-pollinating wasp symbosis. Each pair of fig and pollinating wasp possesses its distinctive coevolutionary history, and there are more than 750 pairs across the globe, which provide rich materials to explore the coevolutionary process and mechanism between plants and animals. The integrated study of formation, maintenance and breakdown mechanisms of the host-specificity will contribute to the understanding of fig-fig-pollinating wasp mutualism, and the coevolutionary process and mechanism between plants and animals.

Key words: fig, fig pollinating wasp, one-to-one rule, cryptic species, copollinator, pollinator sharing

[1] Berg CC (1989) Classification and distribution of Ficus. Experientia, 45, 605-611.
doi: 10.1007/BF01975677
[2] Berg CC, Corner EJH (2005) Moraceae (Ficus). In: Flora Malesiana (ed Nooteboom HP), pp. 340-342. National Herbarium of the Netherlands, Leiden.
[3] Berg CC, Wiebes JT (1992) African fig trees and fig wasps. Verhandelingen der Koninklijke Nederlandsche (Nederland-se) Akademie van Wetenschappen, 89, 1-298.
[4] Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148-155.
doi: 10.1016/j.tree.2006.11.004 pmid: 17129636
[5] Boucek Z, Watsham A, Wiebes JT (1981) The fig wasp fauna of the receptacles of Ficus thonningii (Hymenoptera, Chalcidoidea). Tijdschrift Voor Entomologie, 124, 149-233.
[6] Bruno JF, Cardinale BJ (2008) Cascading effects of predator richness. Frontiers in Ecology and the Environment, 6, 539-546.
doi: 10.1890/070136
[7] Chen Y, Compton SG, Liu M, Chen XY (2012) Fig trees at the northern limit of their range: The distributions of cryptic pollinators indicate multiple glacial refugia. Molecular Ecology, 21, 1687-1701.
doi: 10.1111/j.1365-294X.2012.05491.x pmid: 22335780
[8] Chen Y, Li HQ, Liu M, Chen XY (2010) Species-specificity and coevolution of figs and their pollinating wasps. Biodiversity Science, 18, 1-10. (in Chinese with English abstract)
doi: 10.3724/SP.J.1003.2010.001
[陈艳, 李宏庆, 刘敏, 陈小勇 (2010) 榕-传粉榕小蜂间的专一性与协同进化. 生物多样性, 18, 1-10.]
doi: 10.3724/SP.J.1003.2010.001
[9] Compton SG, Holton KC, Rashbrook VK, van Noort S, Vincent SL, Ware AB (1991) Studies on Ceratosolen galili, a non-pollinating Agaonid fig wasp. Biotropica, 23, 188-194.
doi: 10.2307/2388305
[10] Cook JM, Rasplus JY (2003) Mutualists with attitude: Coevolving fig wasps and figs. Trends in Ecology & Evolution, 18, 241-248.
doi: 10.1016/S0169-5347(03)00062-4
[11] Cook JM, Segar ST (2010) Speciation in fig wasps. Ecological Entomology, 35, 54-66.
doi: 10.1111/een.2010.35.issue-s1
[12] Corner EJH (1965) Check-list of Ficus in Asia and Australasia, with keys to identification. The Gardens’ Bulletin Singapore, 21, 1-186.
[13] Cornille A, Underhill JG, Cruaud A, Hossaert-McKey M, Johnson SD, Tolley KA, Kiellberg F, van Noort S, Proffit M (2011) Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: Insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proceedings of the Royal Society of London B: Biological Sciences, 279, 1731-1739.
doi: 10.1098/rspb.2011.1972 pmid: 22130605
[14] Cruaud A, Jabbour-Zahab R, Genson G, Cruaud C, Couloux A, Kjellberg F, van Noort S, Rasplus JY (2010) Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approach. Cladistics, 26, 359-387.
doi: 10.1111/j.1096-0031.2009.00291.x
[15] Cruaud A, R?nsted N, Chantarasuwan 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 YQ, Pereira RAS, Schramm T, Ubaidillah R, van Noort S, Weiblen GD, Yang DR, Yodpinyanee A, Libeskind-Hadas R, Cook JM, Rasplus JY, Savolainen V (2012) An extreme case of plant-insect co-diversification: Figs and fig-pollinating wasps. Systematic Biology, 61, 1029-1047.
doi: 10.1093/sysbio/sys068 pmid: 22848088
[16] 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 Evolutionary Biology, 14, 189.
doi: 10.1186/s12862-014-0189-9 pmid: 4172794
[17] Galil J, Eisikowitch D (1968) On the pollination ecology of Ficus sycomorus in East Africa. Ecology, 49, 259-269.
doi: 10.2307/1934454
[18] Galil J, Eisikowitch D (1969) Further studies on the pollination in Ficus sycomorus L. (Hymenoptera, Clacidoidea, Agaonidae). Tijdschrift Voor Entomologie, 112, 1-13.
[19] Grandi G (1916) Gli Agaonini (Hymenoptera Chalcididae) raccolti nell’Africa occidentale dal Prof. F. Silvestri. Bollettino del Laboratorio di Zoologia Portici, 10, 121-286.
[20] Grandi G (1922) Identification of some fig insects (Hymenoptera) from the British Museum (Natural History). Bulletin of Entomological Research, 13, 295-299.
doi: 10.1017/S0007485300045387
[21] Grandi G (1927) Hyménopteres sycophiles récoltés aux iles Philippines par CF Baker, I. Agaonini. Philippine Journal of Science, 33, 309-329.
[22] Haine ER, Martin J, Cook JM (2006) Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evolutionary Biology, 6, 83.
doi: 10.1186/1471-2148-6-83 pmid: 1626083
[23] Harrison RD (2005) Figs and the diversity of tropical rainforests. BioScience, 55, 1053-1064.
doi: 10.1641/0006-3568(2005)055[1053:FATDOT]2.0.CO;2
[24] Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences, 270, S96-S99.
doi: 10.1098/rsbl.2003.0025 pmid: 12952648
[25] Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biology, 2, 1657-1663.
[26] Herre EA, Machado CA, Bermingham E, Nason JD, Windsor DM, McCafferty SS, van Houten W, Bachmann K (1996) Molecular phylogenies of figs and their pollinator wasps. Journal of Biogeography, 23, 521-530.
doi: 10.1111/j.1365-2699.1996.tb00014.x
[27] Janzen DH (1979) How to be a fig. Annual Review of Ecology and Systematics, 10, 13-51.
doi: 10.1146/
[28] Johri BM, Konar RN (1955) A contribution to the morphology and embryology of Ficus religiosa Linn. Current Science, 24, 382-385.
[29] Joseph KL (1953) Contributions to our knowledge of fig insects (Chalcidoidea: parasitic Hymenoptera) from India. IV. Descriptions of three new and records of four known species of Agaonini. Agra University Journal of Research, 2, 267-284.
[30] Kerdelhué C, Clainche IL, Rasplus JY (1999) Molecular phylogeny of the Ceratosolen species pollinating Ficus of the subgenus Sycomorus sensu stricto: Biogeographical history and origins of the species-specificity breakdown cases. Molecular Phylogenetics and Evolution, 11, 401-414.
doi: 10.1006/mpev.1998.0590
[31] Kerdelhué C, Hochberg ME, Rasplus JY (1997) Active pollination of Ficus sur by two sympatric fig wasp species in West Africa. Biotropica, 29, 69-75.
doi: 10.1111/j.1744-7429.1997.tb00007.x
[32] Lin RC, Yeung CKL, Fong JJ, Tzeng HY, Li SH (2011) The lack of pollinator specificity in a dioecious fig tree: Sympatric fig-pollinating wasps of Ficus septica in Southern Taiwan. Biotropica, 43, 200-207.
doi: 10.1111/j.1744-7429.2010.00686.x
[33] Liu GX, Yang DR, Peng YQ, Compton SG (2015) Complementary fruiting phenologies facilitate sharing of one pollinator fig wasp by two fig trees. Journal of Plant Ecology, 8, 197-206.
doi: 10.1093/jpe/rtv022
[34] Liu M (2014) Divergence and Comparative Phylogeography of Ficus pumila and Its Pollinating Wasps (Wiebesia spp.). PhD dissertation, East China Normal University, Shanghai. (in Chinese with English abstract)
[刘敏 (2014) 薜荔(Ficus pumila)及其传粉小蜂(Wiebesia spp.)的分化与比较亲缘地理学. 博士学位论文, 华东师范大学, 上海.]
[35] Liu M, Zhao R, Chen Y, Zhang J, Compton SG, Chen XY (2014) Competitive exclusion among fig wasps achieved via entrainment of host plant flowering phenology. PLoS ONE, 9, e97783.
doi: 10.1371/journal.pone.0097783 pmid: 4029822
[36] Machado CA, Jousselin E, Kjellberg F, Compton SG, Herre EA (2001) Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proceedings of the Royal Society of London B: Biological Sciences, 268, 685-694.
doi: 10.1098/rspb.2000.1418
[37] Martinson EO, Jandér KC, Peng YQ, Chen HH, Machado CA, Arnold AE, Herre EA (2014) Relative investment in egg load and poison sac in fig wasps: Implications for physiological mechanisms underlying seed and wasp production in figs. Acta Oecologica, 57, 58-66.
doi: 10.1016/j.actao.2013.07.009
[38] Mayr G (1885) Feigenwespen. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien, 35, 147-250.
[39] Michaloud G, Carriere S, Kobbi M (1996) Exceptions to the one : one relationship between African fig trees and their fig wasp pollinators: Possible evolutionary scenarios. Journal of Biogeography, 23, 513-520.
doi: 10.1111/j.1365-2699.1996.tb00013.x
[40] Michaloud G, Michaloud-Pelletier S, Wiebes JT, Berg CC (1985) The co-occurrence of two pollinating species of fig wasp and one species of fig. Proceedings of the Koninklijke Nederlandse Akademie van Wetenscahppen, Series C, 88, 93-119.
[41] Moe AM, Rossi DR, Weiblen GD (2011) Pollinator sharing in dioecious figs (Ficus: Moraceae). Biological Journal of the Linnean Society, 103, 546-558.
doi: 10.1111/j.1095-8312.2011.01669.x
[42] Moe AM, Weiblen GD (2010) Molecular divergence in allopatric Ceratosolen (Agaonidae) pollinators of geographically widespread Ficus (Moraceae) species. Annals of the Entomological Society of America, 103, 1025-1037.
doi: 10.1603/AN10083
[43] Molbo D, Krieger MJB, Herre EA, Keller L (2002) Species-diagnostic microsatellite loci for the fig wasp genus Pegoscapus. Molecular Ecology Resources, 2, 440-442.
doi: 10.1046/j.1471-8286.2002.00268.x
[44] Molbo D, Machado CA, Sevenster JG, Keller L, Herre EA (2003) Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proceedings of the National Academy of Sciences,USA, 100, 5867-5872.
doi: 10.1073/pnas.0930903100 pmid: 12714682
[45] Müller F (1886) Feigenwespen. Kosmos (Stuttgart), 18, 55-62.
[46] Parrish TL, Koelewijn HP, van Dijk PJ, Kruijt M (2003) Genetic evidence for natural hybridization between species of dioecious Ficus on island populations. Biotropica, 35, 333-343.
doi: 10.1111/btp.2003.35.issue-3
[47] Peng YQ, Compton SG, Yang DR (2010) The reproductive success of Ficus altissima and its pollinator in a strongly seasonal environment: Xishuangbanna, Southwestern China. Plant Ecology, 209, 227-236.
doi: 10.1007/s11258-009-9690-4
[48] Peng YQ, Duan ZB, Yang DR, Rasplus JY (2008) Co-occurrence of two Eupristina species on Ficus altissima in Xishuangbanna, SW China. Symbiosis, 45, 9-14.
[49] Pothasin P, Compton SG, Wangpakapattanawong P (2016) Seasonality of leaf and fig production in Ficus squamosa, a fig tree with seeds dispersed by water. PLoS ONE, 11, e0152380.
doi: 10.1371/journal.pone.0152380 pmid: 4807038
[50] Ramírez BW (1970a) Taxonomic and biological studies of neotropical fig wasps (Hymenoptera: Agaonidae). The University of Kansas Science Bulletin, 49, 1-44.
doi: 10.5962/bhl.part.9196
[51] Ramírez BW (1970b) Host specificity of fig wasps (Agaonidae). Evolution, 24, 680-691.
doi: 10.1111/evo.1970.24.issue-4
[52] Rasplus JY (1996) The one-to-one species-specificity of the Ficus-Agaoninae mutualism: How casual? In: The Biodiversity of African Plants (eds van der Maesen LJG, van der Burgt XM, van Medenbach de Rooy JM), pp. 639-649. Kluwer Academic Publishers, Wageningen.
[53] R?nsted N, Weiblen GD, Clement W, Zerega N, Savolainen V (2008) Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualisms. Symbiosis, 45, 45-56.
doi: 10.1634/stemcells.2008-0642
[54] Shanahan M, So S, Compton SG, Corlett R (2001) Fig-eating by vertebrate frugivores: A global review. Biological Reviews, 76, 529-572.
[55] Su Z, 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 analysis. Symbiosis, 45, 73-81.
doi: 10.1634/stemcells.2008-0642
[56] Sun XJ, Xiao JH, Cook JM, Feng G, Huang DW (2011) Comparisons of host mitochondrial, nuclear and endosymbiont bacterial genes reveal cryptic fig wasp species and the effects of Wolbachia on host mtDNA evolution and diversity. BMC Evolutionary Biology, 11, 86.
doi: 10.1186/1471-2148-11-86
[57] Sutton TL, DeGabriel JL, Riegler M, Cook JM (2017) Local coexistence and genetic isolation of three pollinator species on the same fig tree species. Heredity, 118, 486-490.
doi: 10.1038/hdy.2016.125 pmid: 28074845
[58] Tsai L, Hayakawa H, Fukuda T, Yokoyama J (2015) A breakdown of obligate mutualism on a small island: An interspecific hybridization between closely related fig species (Ficus pumila and Ficus thunbergii) in Western Japan. American Journal of Plant Sciences, 6, 126-131.
doi: 10.4236/ajps.2015.61014
[59] Wachi N, Kusumi J, Tzeng HY, Su ZH (2016) Genome-wide sequence data suggest the possibility of pollinator sharing by host shift in dioecious figs (Moraceae, Ficus). Molecular Ecology, 25, 5732-5746.
doi: 10.1111/mec.13876 pmid: 27706883
[60] Warren M, Robertson MP, Greeff JM (2010) A comparative approach to understanding factors limiting abundance patterns and distributions in a fig tree-fig wasp mutualism. Ecography, 33, 148-158.
doi: 10.1111/j.1600-0587.2009.06041.x
[61] Weiblen GD (2001) Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondria DNA sequences and morphology. Systematic Biology, 50, 243-267.
doi: 10.1080/10635150120131 pmid: 12116930
[62] Weiblen GD, Bush GL (2002) Speciation in fig pollinators and parasites. Molecular Ecology, 11, 1573-1578.
doi: 10.1046/j.1365-294X.2002.01529.x pmid: 12144676
[63] Wiebes JT (1963) Taxonomy and host preferences of Indo-Australian fig wasps of the genus Ceratosolen (Agaonidae). Tijdeschrift Voor Entomologie, 106, 1-112.
[64] Wiebes JT (1964) Fig wasps from Israeli Ficus sycomorus and related East African species (Hymenoptera, Chalcidoidea: Agaonidae). Entomologische Berichten Amsterdam, 24, 187-191.
[65] Wiebes JT (1994) The Indo-Australian Agaoninae (pollinators of figs). Verhandelingen der Koninklijke Nederlandsche (Nederlandse) Akademie van Wetenschappen, 92, 1-208.
[66] Wiebes JT, Compton SG (1990) Agaonidae (Hymenoptera Chalcidoidea) and Ficus (Moraceae): Fig wasps and their figs. VI. (Africa concluded). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen (C), 93, 203-222.
[67] Xu ZF (1994) Ficus—A keystone plant species in the tropical rain forests ecosystem of south Yunnan. Chinese Biodiversity, 2, 21-23. (in Chinese)
[许再富 (1994) 榕树──滇南热带雨林生态系统中的一类关键植物. 生物多样性, 2, 21-23.]
[68] Yang LY, Machado CA, Dang XD, Peng YQ, Yang DR, Zhang DY, Liao WJ (2015) The incidence and pattern of copollinator diversification in dioecious and monoecious fig. Evolution, 69, 294-304.
doi: 10.1111/evo.12584 pmid: 4328460
[69] Zhang DY, Hanski I (1998) Sexual reproduction and stable coexistence of identical competitors. Journal of Theoretical Biology, 193, 465-473.
doi: 10.1006/jtbi.1998.0712 pmid: 9735273
[70] Zhang DY, Lin K, Hanski I (2004) Coexistence of cryptic species. Ecology Letters, 7, 165-169.
doi: 10.1111/ele.2004.7.issue-3
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[1] Haiyan Pei, Xinchun Lin, Wei Fang, Lichun Huang. A Preliminary Study of Somatic Embryogenesis of Phyllostachys violascens In Vitro[J]. Chin Bull Bot, 2011, 46(2): 170 -178 .
[2] Lingcheng Jian;Hong Wang. Ca2+ Signaling in Plant Cell Response and Adaptation to Low Temperature, Drought and Salt Stresses[J]. Chin Bull Bot, 2008, 25(03): 257 -267 .
[3] Hu Wen-xin. An experiment of graft of Cycas guizhouensis[J]. Chin Bull Bot, 1995, 12(专辑): 78 .
[4] . Chemical Composition and Antibacterial Activities of the Essential Oils Isolated from Leaves of Mentha × piperita, M. haplocalyx and M. × gentilis[J]. Chin Bull Bot, 2011, 46(1): 37 -43 .
[5] Zhiyang Zhang Xinbo Chen Yu Zhang Songhua Long Yuan Gao Ailing Liu. Highly Efficient Adventitious Shoot Induction from Hypocotyl Explants in Linum usitatissimum L.[J]. Chin Bull Bot, 2007, 24(05): 629 -635 .
[6] . [J]. Chin Bull Bot, 2001, 18(01): 1 .
[7] Chen Ze-lian and Wu Qi-gen. The Application of Leaf Venation Features of Dicotyls to Plant Taxonomy[J]. Chin Bull Bot, 1993, 10(增刊): 35 -42 .
[8] Wang Li-hong Yang Han-min. Study on Chromosomal Aberration of Regenerated Plant from Different Developing Ways in Lycium Barbarum[J]. Chin Bull Bot, 1991, 8(增刊): 61 -64 .
[9] Cui Kai-rong;Chen Ke-ming;Wang Xiao-zhe and Wang Ya-fu. Current Reseach on Plant Somatic Embryogenesis[J]. Chin Bull Bot, 1993, 10(03): 14 -20 .
[10] Jiang Yue-ling and Pan Rui-chi. Effects of Indole Butyric Acid, Naphthoxyacatic Acid and PP333 on Root of Hypocotyl Cuttings of Mumg Bean Seedlings[J]. Chin Bull Bot, 1995, 12(增刊): 57 -58 .