Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Article
DOI: 10.11646/phytotaxa.579.1.2
Submitted: 2023-01-12
Published: 2023-01-13

Phylogeny of the Ficus sarmentosa complex (Moraceae) uncovered an omitted species and the rank elevation of F. pubigera var. maliformis

College of Architecture and Urban Planning, Tongji University, 1239 Siping Road, Shanghai 200092, China
College of Architecture and Urban Planning, Tongji University, 1239 Siping Road, Shanghai 200092, China
School of Life Sciences, East China Normal University, 500 Dongchuan Road, Shanghai, 200241, China
School of Life Sciences, East China Normal University, 500 Dongchuan Road, Shanghai, 200241, China
Qingpu Lansheng School, 1588 Zhujiajiao Road, Shanghai, 201713, China
School of Life Sciences, East China Normal University, 500 Dongchuan Road, Shanghai, 200241, China
College of Architecture and Urban Planning, Tongji University, 1239 Siping Road, Shanghai 200092, China
Ficus sect. Plagiostigma species complex phylogenetics new species Eudicots

Abstract

The common breakdown of one-to-one obligate mutualism renders that the hybridization and introgression are relatively universal in the evolutionary history of Ficus, which makes Ficus a difficult taxon taxonomically. The Ficus sarmentosa complex includes 10 species and 10 varieties, and multiple taxonomical issues exist so far due to overlapping and plastic morphological traits together with frequent gene flow. To explore the evolutionary history and taxonomy of the F. sarmentosa complex, three nuclear loci and comprehensive sampling were implemented. The phylogenetic result supported the species statuses of F. pumila, F. howii, F. dinganensis, F. pubigera, and F. anserina. Whereas, the phylogenetic relationships between the varieties and three allies of F. sarmentosa still remain unclear based on the current data. Besides, F. pubigera var. maliformis was elevated as the species ranks and then was named F. yunnanensis. At last, an omitted species was uncovered in the complex and then described with named F. muricata.

References

  1. Aiton, W. (1789) Hortus Kewensis (Vol. III). George Nicol, London, pp. 451. https://doi.org/10.5962/bhl.title.4504

  2. Bentham, G. (1854) Florula Hongkongensis. Hooker’s journal of botany and Kew Garden miscellany 6: 76.

  3. Berg, C.C. & Corner, E.J.H. (2005) Moraceae (Ficus). In: Nooteboom, H.P. (ed.) Flora Malesiana. National Herbarium of the Netherlands, Leiden, pp. 1–730.

  4. Berg, C.C. (2003a) Flora Malesiana precursor for the treatment of Moraceae 3: Ficus subgenus Ficus. Blumea 48: 529–550. https://doi.org/10.3767/000651903X489537

  5. Berg, C.C. (2003b) Flora Malesiana precursor for the treatment of Moraceae 4: Ficus subgenus Synoecia. Blumea 48: 551–571. https://doi.org/10.3767/000651903X489546

  6. Berg, C.C. (2007) Precursory taxonomic studies on Ficus (Moraceae) for the Flora of Thailand. Thai Forest Bulletin 35: 4–28.

  7. Brandis, D. (1874) The forest flora of North-West and Central India. Wm. H. Allen & CO., London, pp. 424.

  8. Bronstein, J.L. & McKey, D. (1989) The fig/pollinator mutualism: a model system for comparative biology. Experientia 45: 601–604. https://doi.org/10.1007/BF01975676

  9. Chang, S.S. (1982) Three new species of the Moraceae from China. Acta Phytotaxonomica Sinica 20: 95–98.

  10. Chang, S.S. (1983) New taxa of Moraceae from China. Guihaia 3: 295–306.

  11. Chang, S.S. (1984) New Taxa of Moraceae from China and Vietnam. Acta Phytotaxonomica Sinica 22: 64–76.

  12. Chang, S.S., Wu, C.Y. & Cao, Z.Y. (1998) Moraceae (Ficus). In: Chang, S.S. & Wu, C.Y. (eds.) Flora Reipublicae Popularis Sinicae. Science Press, Beijing, pp. 66–169.

  13. Chantarasuwan, B., Berg, C.C., Kjellberg, F., Rønsted, N., Garcia, M., Baider, C. & van Welzen, P.C. (2015) A new classification of Ficus subsection Urostigma (Moraceae) based on four nuclear DNA markers (ITS, ETS, G3pdh, and ncpGS), morphology and leaf anatomy. PloS One 10: e0128289. https://doi.org/10.1371/journal.pone.0128289

  14. Compton, S.G., Grehan, K. & Van Noort, S. (2009) A fig crop pollinated by three or more species of agaonid fig wasps. African Entomology 17: 215–222. https://doi.org/10.4001/003.017.0212

  15. Corner, E.J.H. (1960) Taxonomic notes on Ficus L., Asia and Australasia. The Gardens’ Bulletin Singapore 18: 1–69.

  16. Corner, E.J.H. (1965) Check-list of Ficus in Asia and Australasia with keys to identification. The Gardens’ Bulletin Singapore 21: 1–186.

  17. Cruaud, A., Rønsted, N., Chantarasuwan, B., Chou, L.S., Clement, W.L., Couloux, A., Cousins, B., Genson, G., Harrison, R.D., Hanson, P.E., Hossaert-McKey, M., Jabbourzahab, R., Jousselin, E., Kerdelhue, C., Kjellberg, F., Lopez-Vaamonde, C., Peebles, J., Peng, Y.-Q., Pereira, R.A.S., Schramm, T., Ubaidillah, R., Vvan Noort, S., Weiblen, W.D., Yang, D.R., Yodpinyanee, A., Libeskind-Hadas, R., Cook, J.M., Rasplus, J.Y. & Savolainen, V. (2012) An extreme case of plant–insect codiversification: figs and fig-pollinating wasps. Systematic Biology 61: 1029–1047. https://doi.org/10.1093/sysbio/sys068

  18. Darwell, C.T., Al-Beidh, S. & Cook, J.M. (2014) Molecular species delimitation of a symbiotic fig-pollinating wasp species complex reveals extreme deviation from reciprocal partner specificity. BMC Evolutionary Biology 14: 1–10. https://doi.org/10.1186/s12862-014-0189-9

  19. Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.

  20. Franchet, A. & Savatier, L. (1875) Enumeratio plantarum: in Japonia. F. Savy, Parisiis [Paris], pp. 436. https://doi.org/10.5962/bhl.title.75

  21. Hill, D.S. (1967) Figs (Ficus spp.) and fig-wasps (Chalcidoidea). Journal of Natural History 1: 413–434. https://doi.org/10.1080/00222936700770401

  22. Janzen, D.H. (1979) How to be a fig. Annual Review of Ecology Systematics 10: 13–51. https://doi.org/10.1146/annurev.es.10.110179.000305

  23. Jousselin, E., Rasplus, J.Y. & Kjellberg, F. (2003) Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus. Evolution 57: 1255–1269. https://doi.org/10.1111/j.0014-3820.2003.tb00334.x

  24. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285

  25. King, G. (1888) Annals of the Royal botanica garden, Calcutta (Vol. 1). L. Reeve & Co., London, pp. 133–135.

  26. Kizirian, D. & Donnelly, M.A. (2004) The criterion of reciprocal monophyly and classification of nested diversity at the species level. Molecular Phylogenetics Evolution 32: 1072–1076. https://doi.org/10.1016/j.ympev.2004.05.001

  27. Lee, H.H. (2009) Genetic differentiation between Ficus pumila var. pumila and Ficus pumila var. awkeotsang and their pollinators. National Taiwan University, Taibei.

  28. Léveillé, A.A.H. (1915) Flore du Kouy Tcheou. Handwritten materials, Le mans, pp. 431.

  29. Li, G.Y. (2021) Moraceae. In: Hu, X. & Lin, Y.J. (eds.) Flora of Zhejiang. Zhejiang Science and Technology Publisher, Hanzhou, pp. 587–621.

  30. Li, H.Q., Chen, J.Y., Wang, S. & Xiong, S.Z. (2012) Evaluation of six candidate DNA barcoding loci in Ficus (Moraceae) of China. Molecular Ecology Resources 12: 783–790. https://doi.org/10.1111/j.1755-0998.2012.03147.x

  31. Linnaeus, C. (1753) Species Plantarum (Vol. 2). Imprensis Laurentii Salvii, Holmiae [Stockholm], pp. 1059–1060. https://doi.org/10.5962/bhl.title.669

  32. Liu, M. (2013) Divergence and comparative phylogeography of Ficus pumila and its pollinating wasps (Wiebesia spp.). East China Normal University, Shanghai.

  33. Loureiro, J. (1790) Flora Cochinchinensis (Vol. 2). Typis, et expensis academicis, Ulyssipone [Lisboa], pp. 666–667. https://doi.org/10.5962/bhl.title.40199

  34. Lu, J., Gui, P., Lu, Z.L., Zhang, L.F., Tian, H.Z., Gilbert, M.G. & Li, H.Q. (2016) Phylogenetic analysis and taxonomic delimitation of the “hairy-fig” complex of Ficus sect. Eriosycea (Moraceae) in China. Phytotaxa 261: 121–136. https://doi.org/10.11646/phytotaxa.261.2.2

  35. Lu, Z.L., Zhang, Z., Zhou, Q.M., Lu, J., Tian, H.Z. & Li, H.Q. (2017) Molecular analyses of Ficus erecta and its allies within the subsection Frutescentiae (Moraceae). Plant Systematics Evolution 303: 603–614. https://doi.org/10.1007/s00606-017-1393-z

  36. Machado, C.A., Robbins, N., Gilbert, M.T.P. & Herre, E.A. (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proceedings of the National Academy of Sciences of the United States of America 102: 6558–6565. https://doi.org/10.1073/pnas.0501840102

  37. Mahima, K., Sudhakar, J.V. & Ramalingam, S. (2020a) Taxonomic delimitation of endemic Ficus amplocarpa and Ficus dalhousiae complexes (Moraceae) by DNA barcoding. Phytotaxa 436: 21–35. https://doi.org/10.11646/phytotaxa.436.1.2

  38. Mahima, K., Sudhakar, J.V. & Sathishkumar, R. (2020b) Molecular phylogeny of the Ficus virens complex (Moraceae). Genome 63: 597–606. https://doi.org/10.1139/gen-2019-0210

  39. Mahima, K., Umapathy, S., Sudhakar, J.V. & Sathishkumar, R. (2021) Systematic reinstatement of highly sacred Ficus krishnae based on differences in morphology and DNA barcoding from Ficus benghalensis (Moraceae). PhytoKeys 186: 121. https://doi.org/10.3897/phytokeys.186.74086

  40. Maximowicz, C.J. (1881) Diagnoses plantarum novarum asiaticarum. IV. Bulletin de l’Acadeìmie impeìriale des sciences de St.-Peìtersbourg 3: 552.

  41. Merrill, E.D. & Chun, W.Y. (1940) Additions to our knowledge of the Hainan flora, III. Sunyatsenia 5: 43–44.

  42. Miquel, F.A.G. (1848) The London Journal of botany (Vol. 7). Reeve, Benham, and Reeve etc, London, pp. 76–77, 436, 442, 453, 469.

  43. Miquel, F.A.G. (1867) Annales musei botanici Lugduno-batavi. C. G. van der Post, Amstelodami, pp. 289,294.

  44. Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300

  45. Oliver, D. (1889) Ficus foveolata. In: Hooker, W.J. (ed.) Icones plantarum or figures. Longman, Rees, Orme, Brown, Green, & Longman, etc, London, pp. 1824. https://doi.org/10.5962/bhl.title.16059

  46. Pederneiras, L.C., Gaglioti, A.L., Romaniuc-Neto, S. & Mansano, V.F. (2018) The role of biogeographical barriers and bridges in determining divergent lineages in Ficus (Moraceae). Botanical Journal of the Linnean Society 187: 594–613. https://doi.org/10.1093/botlinnean/boy036

  47. Renoult, J.P., Kjellberg, F., Grout, C., Santoni, S. & Khadari, B. (2009) Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evolutionary Biology 9: 1–18. https://doi.org/10.1186/1471-2148-9-248

  48. Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029

  49. Rønsted, N., Weiblen, G.D., Clement, W., Zerega, N. & Savolainen, V. (2008) Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis 45: 45–55.

  50. Rønsted, N., Weiblen, G.D., Cook, J.M., Salamin, N., Machado, C.A. & Savolainen, V. (2005) 60 million years of co-divergence in the fig–wasp symbiosis. Proceedings of the Royal Society B: Biological Sciences 272: 2593–2599. https://doi.org/10.1098/rspb.2005.3249

  51. Roxburgh, W. (1832) Flora Indica, or, Descriptions of Indian plants. W. Thacker, Serampore, pp. 534. https://doi.org/10.5962/bhl.title.590

  52. Sata, N. (1944) A monographic study of the genus Ficus from the point of view of economic botany. Contributions from the Institute of Horticulture and Economic Botany, Faculty of Agriculture, Taihoku Imperial University 32: 1–405.

  53. Singh, V. & Singh, P. (1991) Some new combinations in the flora of Sikkim. Journal of Economic and Taxonomic botany 3: 705–706.

  54. Su, Z.H., Sasaki, A., Kusumi, J., Chou, P.A., Tzeng, H.Y., Li, H.Q. & Yu, H. (2022) Pollinator sharing, copollination, and speciation by host shifting among six closely related dioecious fig species. Communications biology 5: 1–15. https://doi.org/10.1038/s42003-022-03223-0

  55. Thunberg, C.P. (1786) Ficus (Vol. 9). Elias Gedner, Upsaliae, pp. 15. https://doi.org/10.5962/bhl.title.164532

  56. Tnah, L.H., Lee, S.L., Tan, A.L., Lee, C.T., Ng, K.K.S. & Ng, C.H. (2016) Intraspecific classification of Ficus deltoidea Jack subsp. deltoidea (Moraceae) in Peninsular Malaysia based on morphological and molecular variations. Biochemical Systematics Ecology 67: 119–128. https://doi.org/10.1016/j.bse.2016.06.001

  57. 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. https://doi.org/10.4236/ajps.2015.61014

  58. Turland, N.J., Wiersema, J.H., Barrie, F.R., Greuter, W., Hawksworth, D.L., Herendeen, P.S., Knapp, S., Kusber, W.-H., Li, D.Z., Marhold, K., May, T.W., McNeill, J., Monro, A.M., Prado, J., Price, M. & Smith, G. (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017 (Vol. 159). Koeltz Botanical Books, Glashütten, pp. 1–254. https://doi.org/10.12705/Code.2018

  59. Vahl, M. (1806) Enumeratio Plantarum (Vol. 2). Impensis Viduae, Hauniae [Copenhagen], pp. 181–204.

  60. Vaniot, E. & Léveillé, A.A.H. (1907) Memorias de la Real Academia de Ciencias y Artes de Barcelona (Vol. 3). A. López Robert, Impresor, Barcelona, pp. 149.

  61. Wachi, N., Kusumi, J., Tzeng, H.Y. & Su, Z.H. (2016) Genome-wide sequence data suggest the possibility of pollinator sharing by host shift in dioecious figs (Moraceae, Ficus). Molecular Ecology 25: 5732–5746. https://doi.org/10.1111/mec.13876

  62. Wang, G., Zhang, X.T., Herre, E.A., McKey, D., Machado, C.A., Yu, W.B., Cannon, C.H., Arnold, M.L., Pereira, R.A.S. & Ming, R. (2021) Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Nature Communications 12: 1–14. https://doi.org/10.1038/s41467-021-20957-3

  63. Wiebes, J.T. (1979) Co-evolution of figs and their insect pollinators. Annual Review of Ecology Systematics 10: 1–12. https://doi.org/10.1146/annurev.es.10.110179.000245

  64. Yamazaki, T. (1983) Taxonomic review of the Moraceae from Japan, Korea, Taiwan and adjacent areas (2). The Journal of Phytogeography and Taxonomy 31: 1–15.

  65. Yang, C.H. (2015) Genetic Structure of Ficus sarmentosa var. henryi in eastern China and the gene introgression between Ficus pumila and Ficus sarmentosa var. henryi. East China Normal University, Shanghai, pp. 58.

  66. Yokoyama, J. (2006) Ficus. In: Iwatsuki, K., Boufford, D.E. & Ohba, H. (eds.) Flora of Japan. Kodansha LTD, Tokyo, pp. 67–74.

  67. Yu, H., Liao, Y.L., Cheng, Y.F., Jia, Y.J. & Compton, S.G. (2021) More examples of breakdown the 1:1 partner specificity between figs and fig wasps. Botanical studies 62: 1–12. https://doi.org/10.1186/s40529-021-00323-8

  68. Yu, H., Zhao, N.X., Yao, J. & Chen, Y.Z. (2006) The influence of species-specific coevolution of figs and fig wasps on Ficus (Moraceae) classification. Journal of Tropical Subtropical Botany 14: 439–443. https://doi.org/10.3969/j.issn.1005-3395.2006.5.014

  69. Zhang, L.F., Zhang, Z., Wang, X.M., Gao, H.Y., Tian, H.Z. & Li, H.Q. (2018) Molecular phylogeny of the Ficus auriculata complex (Moraceae). Phytotaxa 362: 39–54. https://doi.org/10.11646/phytotaxa.362.1.3

  70. Zhang, Z., Liao, S., Li, H.Q. & Zhang, D.S. (2020a) Identifications and typifications of Ficus pubigera var. maliformis and related names. Phytotaxa 464: 102–108. https://doi.org/10.11646/phytotaxa.464.1.9

  71. Zhang, Z., Wang, X.M., Liao, S., Tian, H.Z. & Li, H.Q. (2019) Taxonomic treatment of the Ficus auriculata complex (Moraceae) and typification of some related names. Phytotaxa 399: 203–208. https://doi.org/10.11646/phytotaxa.399.3.4

  72. Zhang, Z., Wang, X.M., Liao, S., Zhang, J.H. & Li, H.Q. (2020b) Phylogenetic reconstruction of Ficus subg. Synoecia and its allies (Moraceae), with implications on the origin of the climbing habit. Taxon 69: 927–945. https://doi.org/10.1002/tax.12282