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

Lum Tsai¹, Hiroshi Hayakawa², Tatsuya Fukuda³, Jun Yokoyama^4*

¹Graduate Schools of Science and Engineering, Yamagata University, Yamagata, Japan.
²National Institute for Agro-Environmental Sciences, Tsukuba, Ibaraki, Japan.
³Faculty of Agriculture, Kochi University, Nankoku, Kochi, Japan.
⁴Faculty of Science, Yamagata University, Yamagata, Japan.

DOI: 10.4236/ajps.2015.61014                

Abstract

Ficus (Moraceae) is a well-known group with specific pollination mutualisms, and hybridization is considered to be rare. Here, we report the presence of interspecific hybrids between Ficus pumila L. and F. thunbergii Maxim. on Okinoshima, a small island offshore of Shikoku, western Japan. AFLP (amplified fragment length polymorphism of genomic DNA) data suggested that more than one-fourth of individuals of morphological F. pumila were assigned as intermediate genotypes, suggesting hybrids. The hybridization between the two species was introgressive and unidirectional from F. thunbergii to F. pumila. The findings of this study, combined with other previous reports, suggest that the breakdown of mutualistic systems can occur in isolated populations such as those on islands.

Keywords

AFLP, Island, Hybridization, Ficus pumila, Ficus thunbergii, Western Japan

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Corner, E.J.H. (1965) Check-list of Ficus in Asia and Australasia with Keys to Identification. Garden’s Bulletin Singapore, 21, 1-186.
[2]	Berg, C.C. and Wiebes, J.T. (1992) African Fig Trees and Fig Wasps. Koninklijke Nederlandse Akademie van Wetenschappen Verhandelingen Afdeling Natuurkunde, Tweede Reeks, Deel 89, Amsterdam.
[3]	Ramirez, B.W. (1974) Coevolution of Ficus and Agaonidae. Annals of the Missouri Botanical Garden, 61, 770-780. http://dx.doi.org/10.2307/2395028
[4]	Wiebes, J.T. (1979) Co-Evolution of Figs and Their Insect Pollinators. Annual Review of Ecology and Systematics, 10, 1-12. http://dx.doi.org/10.1146/annurev.es.10.110179.000245
[5]	Berg, C.C. (1990) Reproduction and Evolution in Ficus (Moraceae): Traits Connected with the Adequate Rearing of Pollinators. Memoirs of the New York Botanical Garden, 55, 169-185.
[6]	Herre, E.A., Machado, C.A., Bermingham, E., Nason, J.D., Windsor, D.M., McCafferty, S.S., van Houten, W. and Bachmann, K. (1996) Molecular Phylogenies of Figs and Their Pollinator Wasps. Journal of Biogeography, 23, 521-530. http://dx.doi.org/10.1111/j.1365-2699.1996.tb00014.x
[7]	Anstett, M.C., Hossaert-McKey, M. and Kjellberg, F. (1997) Figs and Fig Pollinators: Evolutionary Conflicts in a Coevolved Mutualism. Trends in Ecology and Evolution, 12, 94-98. http://dx.doi.org/10.1016/S0169-5347(96)10064-1
[8]	Machado, C.A., Emmanuelle, J., Kjellberg, F., Compton, S.G. and Herre, E.A. (2001) Phylogenetic Relationships, Historical Biogeography and Character Evolution of Fig-Pollinating Wasps. Proceedings of the Royal Society of London B, 268, 685-694.
[9]	Weiblen, G.D. (2001) Phylogenetic Relationships of Fig Wasps Pollinating Functionally Dioecious Figs Based on Mitochondrial DNA Sequences and Morphology. Systematic Biology, 50, 243-267. http://dx.doi.org/10.1080/10635150151125897
[10]	Weiblen, G.D. and Bush, G.L. (2002) Speciation in Fig Pollinators and Parasites. Molecular Ecology, 11, 1573-1578. http://dx.doi.org/10.1046/j.1365-294X.2002.01529.x
[11]	Cook, J.M. and Rasplus, J.Y. (2003) Mutualists with Attitude: Coevolving Fig Wasps and Figs. Trends in Ecology and Evolution, 18, 241-248. http://dx.doi.org/10.1016/S0169-5347(03)00062-4
[12]	Yokoyama, J. (2003) Cospeciation of Figs and Fig-Wasps: A Case Study of Endemic Species Pairs in the Ogasawara Islands. Population Ecology, 45, 249-256. http://dx.doi.org/10.1007/s10144-003-0166-4
[13]	Arnold, M.L. (1997) Natural Hybridization and Evolution. Oxford University Press, Oxford.
[14]	Rieseberg, L.H. and Carney, S.E. (1998) Plant Hybridization (Tansley Review, 102). New Phytologist, 140, 599-624. http://dx.doi.org/10.1046/j.1469-8137.1998.00315.x
[15]	Moe, A.M. and Weiblen, G.D. (2012) Pollinator-Mediated Reproductive Isolation among Dioecious Fig Species (Ficus, Moraceae). Evolution, 66, 3710-3721. http://dx.doi.org/10.1111/j.1558-5646.2012.01727.x
[16]	Wei, Z.D., Kobmoo, N., Cruaud, A. and Kjellberg, F. (2014) Genetic Structure and Hybridization in the Species Group of Ficus auriculata: Can Closely Related Sympatric Ficus Species Retain Their Genetic Identity While Sharing Pollinators? Molecular Ecology, 23, 3538-3550. http://dx.doi.org/10.1111/mec.12825
[17]	Yamazaki, T. (1983) Taxonomic Review of the Moraceae from Japan, Korea, Taiwan and Adjacent Areas (2). Journal of Phytogeography and Taxonomy, 31, 1-15.
[18]	Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. and Zabeau, M. (1995) AFLP: A New Technique for DNA Fingerprinting. Nucleic Acids Research, 23, 4407-4414. http://dx.doi.org/10.1093/nar/23.21.4407
[19]	Pritchard, J.K., Stephens, M. and Donnelly, P. (2000) Inference of Population Structure Using Multilocus Genotype Data. Genetics, 155, 945-959.
[20]	Falush, D., Stephens, M. and Pritchard, J.K. (2007) Inference of Population Structure Using Multilocus Genotype Date: Dominant Markers and Null Alleles. Molecular Ecology Notes, 7, 574-578. http://dx.doi.org/10.1111/j.1471-8286.2007.01758.x
[21]	Yokoyama, J. and Iwatsuki, K. (1998) A Faunal Survey of Fig-Wasps (Chalcidoidea: Hymenoptera) Distributed in Japan and Their Associations with Figs (Ficus: Moraceae). Entomological Science, 1, 37-46.
[22]	Parrish, T.L., Koelewijn, H.P., van Dijk, P.J. and Kruijk, M. (2003) Genetic Evidence for Natural Hybridization between Species of Dioesious Ficus on Island Populations. Biotropica, 35, 333-343. http://dx.doi.org/10.1111/j.1744-7429.2003.tb00587.x
[23]	Janzen, D.H. (1979) How to Be a Fig. Annual Review of Ecology and Systematics, 10, 13-51. http://dx.doi.org/10.1146/annurev.es.10.110179.000305
[24]	Kusumi, J., Azuma, H., Tzeng, H.Y., Chou, L.S., Peng, Y.Q., Nakamura, K. and Su, Z.H. (2012) Phylogenetic Analyses Suggest a Hybrid Origin of the Figs (Moraceae: Ficus) that Are Endemic to the Ogasawara (Bonin) Islands, Japan. Molecular Phylogenetics and Evolution, 63, 168-179. http://dx.doi.org/10.1016/j.ympev.2012.01.004