Biodiv Sci ›› 2020, Vol. 28 ›› Issue (11): 1324-1332. DOI: 10.17520/biods.2020234
Special Issue: 传粉生物学; 昆虫多样性与生态功能
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Liyuan Yang1,2,3, Ruiwu Wang4,*()
Received:
2020-06-09
Accepted:
2020-08-06
Online:
2020-11-20
Published:
2020-08-25
Contact:
Ruiwu Wang
Liyuan Yang, Ruiwu Wang. Asymmetric interactions in fig-fig wasp mutualism[J]. Biodiv Sci, 2020, 28(11): 1324-1332.
Fig. 1 The interaction between figs and their fig pollinating wasps. a, the mutualism was based on figs offering nutrition and habitat to the wasp and the wasps pollinating the figs; b, pollination cheating and host sanction lead to antagonism relationship between fig and fig pollinating wasp; c, cooperation or competition between fig and fig pollinating wasp was dependent on the supply of common resource (according to Wang et al, 2011).
雌雄同株 Monoecy | 雌雄异株 Dioecy | 性别功能 Sexual function | ||
---|---|---|---|---|
雄树 Male tree | 雌树 Female tree | |||
雄花发育产物 Product from male flower | 花粉 Pollen | 花粉 Pollen | - | 雄性功能 Male function |
雌花发育产物 Product from female flower | 小蜂 Wasp | 小蜂 Wasp | - | |
种子 Seed | - | 种子 Seed | 雌性功能 Female function |
Table 1 Sex function allocation of fig flower and syconium
雌雄同株 Monoecy | 雌雄异株 Dioecy | 性别功能 Sexual function | ||
---|---|---|---|---|
雄树 Male tree | 雌树 Female tree | |||
雄花发育产物 Product from male flower | 花粉 Pollen | 花粉 Pollen | - | 雄性功能 Male function |
雌花发育产物 Product from female flower | 小蜂 Wasp | 小蜂 Wasp | - | |
种子 Seed | - | 种子 Seed | 雌性功能 Female function |
寄主榕树性系统 Host sexual system | 产卵器长度大于腹部的传粉小蜂种数 Ovipositor is longer than the thorax | 产卵器长度短于腹部的传粉小蜂种数 Ovipositor is shorter than the thorax | 总计 Total |
---|---|---|---|
雌雄同株 Monoecy | 12 | 3 | 15 |
雌雄异株 Dioecy | 0 | 28 | 28 |
总计 Total | 12 | 31 | 43 |
Table 2 Number of pollinating wasp species with different ovipositor length in different fig sexual systems
寄主榕树性系统 Host sexual system | 产卵器长度大于腹部的传粉小蜂种数 Ovipositor is longer than the thorax | 产卵器长度短于腹部的传粉小蜂种数 Ovipositor is shorter than the thorax | 总计 Total |
---|---|---|---|
雌雄同株 Monoecy | 12 | 3 | 15 |
雌雄异株 Dioecy | 0 | 28 | 28 |
总计 Total | 12 | 31 | 43 |
博弈策略 Strategy | 受益方 Winner | 博弈结果 Result | 非对称关系 Asymmetric interaction | 代表性文献 Typical reference |
---|---|---|---|---|
主动传粉 Active pollinating | 榕树 Figs | 榕树节约花粉 Figs produce less pollens | 实力不对称 Asymmetric power | |
传粉欺骗 Pollinator cheating | 小蜂 Wasps | 小蜂减少传粉负担 Wasp takes less burden for carrying pollens | 信息不对称 Asymmetric information | |
寄主惩罚 Host sanction | 榕树 Figs | 防止欺骗者的出现 Reducing the cheating wasps | 实力不对称 Asymmetric power | |
传粉投机者 Speculator | 小蜂 Wasps | 小蜂逃避寄主惩罚 The wasps avoid the host sanction | 信息不对称 Asymmetric information | |
雌树诱骗 Female tree attracts wasp by mimicking male tree | 榕树 Figs | 小蜂失去繁殖机会 Wasps fail to reproduce | 实力不对称 Asymmetric power | |
基因突变产生欺骗者 Mutation causes cheaters | 小蜂 Wasps | 维持种群内投机者比例 Stable proportion of cheaters in population | 进化速率不对称 Asymmetric evolution rates |
Table 3 The asymmetric interaction between fig and fig pollinating wasp during the pollination conflict
博弈策略 Strategy | 受益方 Winner | 博弈结果 Result | 非对称关系 Asymmetric interaction | 代表性文献 Typical reference |
---|---|---|---|---|
主动传粉 Active pollinating | 榕树 Figs | 榕树节约花粉 Figs produce less pollens | 实力不对称 Asymmetric power | |
传粉欺骗 Pollinator cheating | 小蜂 Wasps | 小蜂减少传粉负担 Wasp takes less burden for carrying pollens | 信息不对称 Asymmetric information | |
寄主惩罚 Host sanction | 榕树 Figs | 防止欺骗者的出现 Reducing the cheating wasps | 实力不对称 Asymmetric power | |
传粉投机者 Speculator | 小蜂 Wasps | 小蜂逃避寄主惩罚 The wasps avoid the host sanction | 信息不对称 Asymmetric information | |
雌树诱骗 Female tree attracts wasp by mimicking male tree | 榕树 Figs | 小蜂失去繁殖机会 Wasps fail to reproduce | 实力不对称 Asymmetric power | |
基因突变产生欺骗者 Mutation causes cheaters | 小蜂 Wasps | 维持种群内投机者比例 Stable proportion of cheaters in population | 进化速率不对称 Asymmetric evolution rates |
[1] | Berg CC, Corner EJ, Nooteboom HP (2005) Flora Malesiana (Moraceae-Ficus). National Herbarium Nederland, Leiden. |
[2] |
Bronstein JL (2001) The exploitation of mutualisms. Ecology Letters, 4, 277-287.
DOI URL |
[3] |
Chen C, Song QS, Proffit M, Bessière JM, Li ZB, Hossaert-McKey M (2009) Private channel: A single unusual compound assures specific pollinator attraction in Ficus semicordata. Functional Ecology, 23, 941-950.
DOI URL |
[4] | 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) |
[ 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.] | |
[5] |
Compton SG, Holton KC, Rashbrook VK, Van Noort S, Vincent SL (1991) Studies of Ceratosolen galili, a non-pollinating agaonid fig wasp. Biotropica, 23, 188-194.
DOI URL |
[6] |
Cook JM, Lopez-Vaamonde C (2001) Fig biology: Turning over new leaves. Trends in Ecology & Evolution, 16, 11-13.
DOI URL |
[7] |
Cook JM, Rasplus J-Y (2003) Mutualists with attitude: Coevolving fig wasps and figs. Trends in Ecology & Evolution, 18, 241-248.
DOI URL |
[8] |
Cook JM, West SA (2005) Figs and fig wasps. Current Biology, 15, R978-R980.
DOI URL PMID |
[9] | Cruaud A, Ronsted N, Chantarasuwan B, Chou LS, Clement WL, Couloux A, Cousins B, Genson G, Harrison RD, Hanson PE (2012) An extreme case of plant-insect co-diversification: Figs and fig-pollinating wasps. Systematic Biology, 61, 1029-1047. |
[10] | Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conservation Biology, 10, 1500-1508. |
[11] | Galil J, Eisikowitch D (1968) On the pollination ecology of Ficus sycomorus in East Africa. Ecology, 49, 259-269. |
[12] | Ganeshaiah KN, Kathuria P, Shaanker RU, Vasudeva R (1995) Evolution of style-length variability in figs and optimization of ovipositor length in their pollinatior wasps: A coevolutionary model. Journal of Genetics, 74, 25-39. |
[13] |
Ghana S, Suleman N, Compton SG (2017) Style length variation in male and female figs: Development, inheritance, and control of pollinator oviposition. Entomologia Experimentalis et Applicata, 162, 41-50.
DOI URL |
[14] |
Gu D, Compton SG, Peng YQ, Yang DR (2012) “Push” and “pull” responses by fig wasps to volatiles released by their host figs. Chemoecology, 22, 217-227.
DOI URL |
[15] | Guan JM, Peng YQ, Yang DR (2007) Host sanctions in fig-fig wasp mutualism. Biodiversity Science, 15, 1569-1574. (in Chinese with English abstract) |
[ 管俊明, 彭艳琼, 杨大荣 (2007) 榕-蜂互惠关系中榕树对未传粉榕小蜂的惩罚效应. 生物多样性, 15, 626-632.] | |
[16] |
Haine ER, Martin J, Cook JM (2006) Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evolutionary Biology, 6, 83-94.
DOI URL PMID |
[17] | Herre EA (1985) Sex ratio adjustment in fig wasps. Science, 228, 896-898. |
[18] | Herre EA (1987) Optimality, plasticity and selective regime in fig wasp sex ratios. Nature, 329, 627-629. |
[19] | Herre EA, Jander KC, Machado CA (2008) Evolutionary ecology of figs and their associates: Recent progress and outstanding puzzles. Annual Review of Ecology, Evolution, and Systematics, 39, 439-458. |
[20] |
Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: Exploring the paths between conflict and cooperation. Trends in Ecology & Evolution, 14, 49-53.
URL PMID |
[21] |
Hossaert-McKey M, Proffit M, Soler CCL, Chen C, Bessiere JM, Schatz B, Borges RM (2016) How to be a dioecious fig: Chemical mimicry between sexes matters only when both sexes flower synchronously. Scientific Reports, 6, 21236.
DOI URL PMID |
[22] | Hossaert-McKey M, Soler C, Schatz B, Proffit M (2010) Floral scents: Their roles in nursery pollination mutualisms. Chemoecology, 20, 75-88. |
[23] | Huang JF, Xu R, Peng YQ (2018) Progress on the breakdown of one-to-one rule in symbiosis of figs and their pollinating wasps. Biodiversity Science, 26, 295-303. (in Chinese with English abstract) |
[ 黄建峰, 徐睿, 彭艳琼 (2018) 榕-传粉榕小蜂非一对一共生关系的研究进展. 生物多样性, 26, 295-303.] | |
[24] |
Jander KC, Dafoe A, Herre EA (2016) Fitness reduction for uncooperative fig wasps through reduced offspring size: A third component of host sanctions. Ecology, 97, 2491-2500.
DOI URL PMID |
[25] | Jander KC, Herre EA (2010) Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism. Proceedings of the Royal Society B: Biological Sciences, 277, 1481-1488. |
[26] | Jander KC, Herre EA (2016) Host sanctions in Panamanian Ficus are likely based on selective resource allocation. American Journal of Botany, 103, 1753-1762. |
[27] |
Jander KC, Herre EA, Simms EL, Irwin R (2012) Precision of host sanctions in the fig tree-fig wasp mutualism: Consequences for uncooperative symbionts. Ecology Letters, 15, 1362-1369.
DOI URL PMID |
[28] |
Jander KC, Steidinger BS (2017) Why mutualist partners vary in quality: Mutation-selection balance and incentives to cheat in the fig tree-fig wasp mutualism. Ecology Letters, 20, 922-932.
URL PMID |
[29] | Janzen DH (1979) How to be a fig. Annual Review of Ecology and Systematics, 10, 13-51. |
[30] | Kjellberg F, Jousselin E, Bronstein JL, Patel A, Yokoyama J, Rasplus JY (2001) Pollination mode in fig wasps: The predictive power of correlated traits. Proceedings of the Royal Society B: Biological Sciences, 268, 1113-1121. |
[31] |
Li ZT, Peng YQ, Wen XL, Jander KC (2016) Selective resource allocation may promote a sex ratio in pollinator fig wasps more beneficial for the host tree. Scientific Reports, 6, 35159.
DOI URL PMID |
[32] | Machado CA, Robbins N, Gilbert MTP, Herre EA (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proceedings of the National Academy of Sciences, USA, 102, 6558-6565. |
[33] | Moe AM, Clement W, Weiblen GD (2012) Rapid evolution of pollinator-mediated plant reproductive isolation. In: Rapidly Evolving Genes and Genetic Systems (eds Singh RS, Xu J, Kulathinal RJ), pp. 266-273. Oxford University Press, Oxford. |
[34] | 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. |
[35] | Murray MG (1985) Figs (Ficus spp.) and fig wasps (Chalcidoidea, Agaonidae): Hypotheses for an ancient symbiosis. Biological Journal of the Linnean Society, 26, 69-81. |
[36] | 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. |
[37] | Proffit M, Schatz B, Bessiere JM, Chen C, Soler C, Hossaert- Mckey M (2008) Signalling receptivity: Comparison of the emission of volatile compounds by figs of Ficus hispida before, during and after the phase of receptivity to pollinators. Symbiosis, 45, 15-24. |
[38] |
Rubin BER, Moreau CS (2016) Comparative genomics reveals convergent rates of evolution in ant-plant mutualisms. Nature Communications, 7, 12679.
URL PMID |
[39] |
Sharp PM, Li WH (1989) On the rate of DNA sequence evolution in Drosophila. Journal of Molecular Evolution, 28, 398-402.
DOI URL PMID |
[40] | Smith JM (1982) Evolution and the theory of games. Cambridge University Press, Cambridge. |
[41] |
Soler CCL, Proffit M, Bessiere JM, Hossaert-McKey M, Schatz B (2012) Evidence for intersexual chemical mimicry in a dioecious plant. Ecology Letters, 15, 978-985.
URL PMID |
[42] |
Souto-Vilarós D, Machac A, Michalek J, Darwell CT, Segar ST (2019) Faster speciation of fig-wasps than their host figs leads to decoupled speciation dynamics: Snapshots across the speciation continuum. Molecular Ecology, 28, 3958-3976.
DOI URL PMID |
[43] |
Thompson RCA (2013) Parasite zoonoses and wildlife: One health, spillover and human activity. International Journal for Parasitology, 43, 1079-1088.
DOI URL PMID |
[44] | Wang B, Geng XZ, Ma LB, Cook JM, Wang RW (2014) A trophic cascade induced by predatory ants in a fig-fig wasp mutualism. Journal of Animal Ecology, 83, 1149-1157. |
[45] |
Wang RW, Dunn DW, Sun BF (2014) Discriminative host sanctions in a fig-wasp mutualism. Ecology, 95, 1384-1393.
DOI URL PMID |
[46] |
Wang RW, Ridley J, Sun BF, Zheng Q, Dunn DW, Cook J, Shi L, Zhang YP, Yu DW (2009) Interference competition and high temperatures reduce the virulence of fig wasps and stabilize a fig-wasp mutualism. PLoS ONE, 4, e7802.
URL PMID |
[47] | Wang RW, Sun BF, Yang Y (2015a) Discriminative host sanction together with relatedness promote the cooperation in fig-fig wasp mutualism. Journal of Animal Ecology, 84, 1133-1139. |
[48] | Wang RW, Sun BF, Zheng Q, Shi L, Zhu LX (2011) Asymmetric interaction and indeterminate fitness correlation between cooperative partners in the fig-fig wasp mutualism. Journal of the Royal Society Interface, 8, 1487-1496. |
[49] |
Wang RW, Wen XL, Chen C, Shi L, Compton SG (2015b) Spatial heterogeneity and host repression in fig-fig wasp mutualism. Science China: Life Sciences, 58, 492-500.
DOI URL PMID |
[50] |
Weiblen GD (2002) How to be a fig wasp. Annual Review of Entomology, 47, 299-330.
DOI URL PMID |
[51] |
Weiblen GD (2004) Correlated evolution in fig pollination. Systematic Biology, 53, 128-139.
URL PMID |
[52] | Xu R, Zhang Y, Peng YQ, Yang DR (2016) Reproductive characteristics of pollinator and cheater wasps that utilize the female flowers of Ficus altissima. Acta Ecologica Sinica, 36, 1134-1140. (in Chinese with English abstract) |
[ 徐睿, 张媛, 彭艳琼, 杨大荣 (2016) 高榕雌花期传粉榕小蜂和欺骗性小蜂的繁殖特点. 生态学报, 36, 1134-1140.] | |
[53] | Yang DR, Xu L, Peng YQ, Wei ZD, Duan ZB (2004) Species composition and diversity of fig wasps and figs in Yunnan. Biodiversity Science, 12, 611-617. (in Chinese with English abstract) |
[ 杨大荣, 徐磊, 彭艳琼, 魏作东, 段柱标 (2004) 云南省榕小蜂和榕树的物种组成及多样性. 生物多样性, 12, 611-617.] | |
[54] |
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 figs. Evolution, 69, 294-304.
DOI URL PMID |
[55] | Yu DW, Ridley J, Jousselin E, Herre EA, Compton SG, Cook JM, Moore JC, Weiblen GD (2004) Oviposition strategies, host coercion and the stable exploitation of figs by wasps. Proceedings of the Royal Society B: Biological Sciences, 271, 1185-1195. |
[56] | Zhang DY (2000) Researches on Theoretical Ecology. Higher Education Press, Beijing. (in Chinese with English abstract) |
[ 张大勇 (2000) 理论生态学研究. 高等教育出版社, 北京.] | |
[57] | Zhang DY, Lin K, Hanski I (2004) Coexistence of cryptic species. Ecology Letters, 7, 165-169. |
[58] | Zhang T, Miao BG, Wang B, Peng YQ, Darwell CT (2019) Non-pollinating cheater wasps benefit from seasonally poor performance of the mutualistic pollinating wasps at the northern limit of the range of Ficus microcarpa. Ecological Entomology, 044, 844-848. |
[59] |
Zhang XW, Dunn DW, Wen XL, Sun BF, Wang RW (2019) Differential deployment of sanctioning mechanisms by male and female host trees in a gynodioecious fig-wasp mutualism. Ecology, 100, e02597.
DOI URL PMID |
[60] | Zhang Y, Peng YQ, Yang DR (2014) Effects of foundress number, foundresses entry interval and non-pollinating wasps on clutch size and offspring sex ratio of pollinating fig wasps (Hymenoptera: Agaonidae). Acta Entomologica Sinica, 57, 587-593. (in Chinese with English abstract) |
[ 张媛, 彭艳琼, 杨大荣 (2014) 母代雌蜂数、进果时间及非传粉小蜂对传粉榕小蜂后代数量及性比的影响. 昆虫学报, 57, 587-593.] |
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