Research Paper

Genetic data revealed co-diversification and host switching in the Wiebesia pumilae species complex, pollinators of Ficus pumila

Bai-Wei Lo, Hunrg-Yi Wang

Published on: 18 August 2021

Page: 345 - 352

DOI: 10.6165/tai.2021.66.345

Abstract

Figs and their pollinating fig wasps constitute a classic example of co-evolution. Recent molecular studies revealed that multiple cryptic fig wasp species may interact with single or different fig hosts; these species include pollinators associated with Ficus pumila. However, previous studies focused on different geographical ranges and fig varieties. The full evolutionary picture of F. pumila and its pollinating wasp, Wiebesia pumilae, has not been unraveled. Here, we collected mitochondrial COI sequences from the literature and studied the evolutionary history and phylogeography of the pollinating fig wasps of F. pumila L. var. pumila (creeping fig) and F. pumila var. awkeotsang (Makino) Corner (jelly fig). The W. pumilae contains three distinct lineages, of which Sp. 3 is mostly associated with F. pumila var. awkeotsang and Sp. 1 and Sp. 2 exclusively with F. pumila var. pumila. Wiebesia sp. 3 showed no genetic differentiation between sample collected from China and Taiwan. Besides, Sp. 3 samples from China exhibits only approximately 50% of genetic diversity compared to samples from Taiwan, suggesting Sp. 3 in China was recently introduced from Taiwan. Our study clarified the co-evolutionary relationships among F. pumila varieties and their pollinators, while showing how human activities have influenced their distribution. We also provide support for the endemism of both F. pumila var. awkeotsang and Sp. 3 in Taiwan.

Keyword: Co-evolution, Ficus pumila var. awkeotsang, fig wasp, host switching, introduced species, phylogeography

Literature Cited

Benson, Dennis A., Mark Cavanaugh, Karen Clark, Ilene Karsch-Mizrachi, David J. Lipman, James Ostell, and Eric W. Sayers. 2017. GenBank. Nucleic Acids Res. 45(D1): D37–42.
DOI: 10.1093/nar/gkw1070View Article Google Scholar

Chen, Y., S.G. Compton, M. Liu, and X.-Y. Chen. 2012. Fig trees at the northern limit of their range: the distributions of cryptic pollinators indicate multiple glacial refugia. Mol. Ecol. 21(7): 1687–1701.
DOI: 10.1111/j.1365-294X.2012.05491.xView Article Google Scholar

Chen, Y., H.-Q. Li, S.-J. Ruan, and W.-L. Ma. 2008. Pollination of a cultivated fig, Ficus pumila var. awkeotsang, in South China. Symbiosis 45(1): 33–36.

Chen, Y., H.Q. Li, and W.L. Ma. 2002. The reproductive character of Ficus pumila var. pumila, F. pumila var. awkeotsang and their pollinators. Acta Phytoecologica Sinica 26(1): 58–63.

Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9(10): 1657–1659.
DOI: 10.1046/j.1365-294x.2000.01020.xView Article Google Scholar

Cook, J.M., and S.T. Segar. 2010. Speciation in fig wasps. Ecol. Entomol. 35: 54–66.
DOI: 10.1111/j.1365-2311.2009.01148.xView Article Google Scholar

Cruaud, A., N. Ronsted, B. Chantarasuwan, L.S. Chou, W.L. Clement, A. Couloux, B. Cousins, G. Genson, R.D. Harrison, P.E. Hanson, M. Hossaert-Mckey, R. Jabbour-Zahab, E. Jousselin, C. Kerdelhu?, F. Kjellberg, C. Lopez-Vaamonde, J. Peebles, Y.Q. Peng, R.A.S. Pereira, T. Schramm, R. Ubaidillah, S.V. Noort, G.D. Weiblen, D.R. Yang, A. Yodpinyanee, R. Libeskind-Hadas, J.M. Cook, J.Y. Rasplus, and V. Savolainen. 2012. An extreme case of plant-insect codiversification: figs and fig-pollinating wasps. Syst. Biol. 61(6): 1029–1047.
DOI: 10.1093/sysbio/sys068View Article Google Scholar

Excoffier, L., P.E. Smouse, and J.M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131(2): 479–491.
DOI: 10.1093/genetics/131.2.479View Article Google Scholar

Excoffier, L. and H.E. L. Lischer. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under linux and windows. Mol. Ecol. Resour. 10(3): 564–567.
DOI: 10.1111/j.1755-0998.2010.02847.xView Article Google Scholar

Herre, E.A., K.C. Jand?r, and C.A. Machado. 2008. Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annu. Rev. Ecol. Evol. Syst. 39(1): 439–458.
DOI: 10.1146/annurev.ecolsys.37.091305.110232View Article Google Scholar

Hsieh, C.F., T.C. Huang, Z.Y. Li, H.C. Lo, H. Ohashi, C.F. Shen, J.C. Wang, and K.C. Yang. 1993. Flora of Taiwan, vol. 2. 2nd ed. 171–174. Editorial Committee, Dept. Bot., NTU, Taipei, Taiwan.

Jackson, A.P., C.A. Machado, N. Robbins, and E.A. Herre. 2008. Multi-locus phylogenetic analysis of Neotropical figs does not support co-speciation with the pollinators: the importance of systematic scale in fig/wasp cophylogenetic studies. Symbiosis 45: 52–72.

Kong, S.-W. 2011. Morphological differences between pollinating fig wasps of Ficus pumila var. pumila and var. awkeotsang (Makino) Corner and their asymmetric host specificity. Master’s thesis, Department of Entymology, National Taiwan University.

Kumar, S., G. Stecher, and K. Tamura. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33(7): 1870–1874.
DOI: 10.1093/molbev/msw054View Article Google Scholar

Larkin, M. A., G. Blackshields, N.P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23(21): 2947–2948.
DOI: 10.1093/bioinformatics/btm404View Article Google Scholar

Leigh, J.W., and D. Bryant. 2015. Popart?: full-feature software for haplotype network construction. Methods Ecol. Evol. 6(9): 1110–1116.
DOI: 10.1111/2041-210X.12410View Article Google Scholar

Lin, R.-C., C.K. L. Yeung, J.J. Fong, H.-Y. Tzeng, and S.-H. Li. 2011. The lack of pollinator specificity in a dioecious fig tree: sympatric fig-pollinating wasps of Ficus septica in southern Taiwan. Biotropica 43(2): 200–207.
DOI: 10.1111/j.1744-7429.2010.00686.xView Article Google Scholar

Lin, T.P., C.C. Liu, C.Y. Yang, R.S. Huang, Y.S. Lee, and S.Y. Chang. 1990. Morphological and biochemical comparison of syconium of Ficus awkeotsang and Ficus pumila. Bull. Taiwan Forest Res. Inst. 5(1): 37–43.
DOI: 10.7075/BTFRI.199003.0037View Article Google Scholar

Liu, M., R. Zhao, Y. Chen, J. Zhang, S.G. Compton, and X.-Y. Chen. 2014. Competitive exclusion among fig wasps achieved via entrainment of host plant flowering phenology. PLoS ONE 9(5): e97783.
DOI: 10.1371/journal.pone.0097783View Article Google Scholar

Machado, C.A., N. Robbins, M. Thomas P. Gilbert, and E.A. Herre. 2005. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. PNAS 102(Suppl 1): 6558–6565.
DOI: 10.1073/pnas.0501840102View Article Google Scholar

Meirmans, P.G. 2006. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60(11): 2399–2402.
DOI: 10.1554/05-631.1View Article Google Scholar

Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3(5): 418–426.
DOI: 10.1093/molbev/msh242View Article Google Scholar

Rasplus, J.Y. 1996. The one-to-one species specificity of the ficus-agaoninae mutualism: how casual? in The Biodiversity of African Plants. 639-649. Springer, Dordrecht, Netherlands.
DOI: 10.1007/978-94-009-0285-5_78View Article Google Scholar

Rodriguez, L.J., A. Bain, L.S. Chou, L. Conchou, A. Cruaud, R. Gonzales, M. Hossaert-Mckey, J.Y. Rasplus, H.Y. Tzeng, and F. Kjellberg. 2017. Diversification and spatial structuring in the mutualism between Ficus septica and its pollinating wasps in insular South East Asia. BMC Evol. Biol. 17(1): 1–12.
DOI: 10.1186/s12862-017-1034-8View Article Google Scholar

Rozas, J., A. Ferrer-Mata, J.C. S?nchez-DelBarrio, S. Guirao-Rico, P. Librado, S.E. Ramos-Onsins, and A. S?nchez-Gracia. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34(12): 3299–3302.
DOI: 10.1093/molbev/msx248View Article Google Scholar

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

Wang, H.-Y., C.-H. Hsieh, C.-G. Huang, S.-W. Kong, H.-C. Chang, H.-H. Lee, W.-K. Wang, S.-L. Chen, H.-Y. Tzeng, and W.-J. Wu. 2013. Genetic and physiological data suggest demographic and adaptive responses in complex interactions between populations of figs (Ficus pumila) and their pollinating wasps (Wiebesia pumilae). Mol. Ecol. 22(14): 3814–3832.
DOI: 10.1111/mec.12336View Article Google Scholar

Weiblen, George D. 2001. Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphology. Syst. Biol. 50(2): 243–267.
DOI: 10.1080/10635150151125897View Article Google Scholar

Wiebes, J.T. 1979. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Evol. Syst. 10(1): 1–12.
DOI: 10.1146/annurev.es.10.110179.000245View Article Google Scholar

Wu, Z.Y., P.H. Raven, and D.Y. Hong. 2003. Flora of China. Volume 5: Ulmaceae through Basellaceae. 69–70. Science Press, Beijing, China and Missouri Botanical Garden Press, St. Louis, USA.
DOI: 10.3100/025.015.0214View Article Google Scholar

Yang, L.-Y., C.A. Machado, X.-D. Dang, Y.-Q. Peng, D.-R. Yang, D.-Y. Zhang, and W.-J. Liao. 2015. The incidence and pattern of copollinator diversification in dioecious and monoecious figs. Evolution 69(2): 294–304.
DOI: 10.1111/evo.12584View Article Google Scholar

Yang, S., Y.L. Chen, W.S. Wu, X.J. Chen, T.T. Bao, J.F. Ye, T.Y. Song, Y.L. Wu, L.S. Chou, and H.Y. Tzeng. 2017. Behavioral responses of Wiebesia pumilae to the female phase fig volatiles of Ficus pumila var. pumila and Ficus pumila var. awkeotsang. Acta Ecologica Sinica 37(21): 7161–7169.