Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

OAI: https://www.revistas.ucr.ac.cr/index.php/rbt/oai
A living fossil Tetrapus fig wasp (Hymenoptera: Agaoninae) developing in extant Neotropical fig species (Moraceae: Ficus, section Pharmacosycea)
PT 64-4 dic 2016
HTML
PDF

Supplementary Files

Untitled

Keywords

Agaoninae
Tetrapus
Hexapus
Ficus
section Pharmacosycea
subsection Petenenses
living fossil wasps.
Chalcidoidea
Agaoninae
Tetrapus
Hexapus
sección Pharmacosycea
fósil viviente.

How to Cite

Ramirez-Benavides, W. (2016). A living fossil Tetrapus fig wasp (Hymenoptera: Agaoninae) developing in extant Neotropical fig species (Moraceae: Ficus, section Pharmacosycea). Revista De Biología Tropical, 64(4), 1721–1735. https://doi.org/10.15517/rbt.v64i4.20808

Abstract

It has been assumed that Tetrapus female wasps (Agaonidae s.s.), the pollinators of the figs of the New World, section Pharmacosycea, are mainly characterized by the presence of one mandibular appendange only, and that it is the most ancestral clade of extant Agaonidae s.s., and the males are tetrapodous. The main objective of this work was to study five Tetrapus morphotypes, whose females have two mandibular appendages and the males are hexapodous, their fig host association and phylogenetic position to the family Agaonidae. The question of which group of fig pollinating wasps and associated figs are the sister to the rest of the pollinating agaonids, and figs respectively remain open. I report a group of New World extant Tetrapus morphotypes (Agaonidae: Agaoninae) provisionally assigned to Hexapus subg. nov. in preparation. Currently, Tetrapus appears as the sister taxon to all other fig pollinating taxa. Howeveer, morphologically, ecologically, geographically and historically Hexapus seems to be the ancestral clade of the extant Agaoninae. Hexapus morphotypes develop in fig species of subsection Petenenses (section Pharmacosycea). In the known extant Tetrapus, the females have one mandibular appendage and the males have reduced one or two short-lobe atrophied non-functional midlegs (tetrapodous). Hexapus females have two free mandibular appendages, and the males have five segmented functional mid-legs (hexapodous). Molecularly Hexapus seems to be the ancestral clade of extant Agaoninae; e.g., a Tetrapus sp. of Ficus crassivenosa was placed by other author as the ancestral clade of 101 wasp species, representing 19 worldwide Agaoninae genera, including four Tetrapus species. In Tetrapus sp. of Ficus crassivenosa, the female has two mandibular appendages and the male is hexapodous. The females of T. apopnus and T. delclosi, preserved in Early to mid-Miocene amber from the Dominican Republic, also have two mandibular appendages and the general morphology of extant Hexapus. I suggest that Hexapus stands up as a living fossil and the sister clade of Tetrapus s.s. The presence of extant Hexapus; as well as extant Tetrapus and their fig host species, especially in South America supports a Southern Gondwanaland origin for both of them, but not a trans-Pacific migrating connection with tropical America for section Pharmacosycea (the host of Tetrapus and Hexapus), a long oceanic dispersal, high levels of stem extinction of Tetrapus or Atlantic land connections, as proposed by other authors. However, lastly it has been assumed that figs and their pollinators arose simultaneously in Eurasia during early Tertiary and spread southwards from it. Most of the morphological and molecular studies of the fig biology of Agaoninae and Ficus, did not include Hexapus morphotypes and their fig hosts, and assumed that Tetrapus is the most ancestral clade of the extant fig pollinating wasps.

https://doi.org/10.15517/rbt.v64i4.20808
HTML
PDF

References

Azuma, H., Harrison, R. D., Nakamura, K., & Su, Z. H. (2010). Molecular phylogenies of figs and fig-pollinating wasps in the Ryukyu and Bonin (Ogasawara) islands, Japan. Genes and Genetic Systems, 85, 177-192.

Berg, C. C. (1989). Clasification and distribution of Ficus. Experientia, 45, 605-611.

Berg, C. C. (2006). The subdivision of Ficus subgenus Pharmacocycea section Pharmacosycea (Moraceae). Blumea, 51, 147-151.

Berg, C. C. (2009). Flora of Ecuador No 85, 27C. In G. Harling, C., Persson, C. (Eds.), Moraceae (Ficus). Göteborg: University of Gothenburg.

Berg, C. C. & Corner, E. J. H. (2005). Flora Malesiana (Moraceae-Ficus). Vol. 17, Part 2.

Bouček, Z. (1988). Australasian Chalcidoidea (Hymenoptera): A biosystematic revision of genera of fourteen families, with a reclassification of species. Wallingford, UK: CAB International.

Bouček, Z. (1993). The genera of chalcidoid wasps from Ficus fruit in the New World. Journal of Natural History, 27, 173-217.

Burger, W. (1977). Flora costaricensis. Family 52. Moraceae. Fieldiana. Botany, 40, 84-185.

Chen, C. H., & Chou, L. Y. (1997). The Blastophagini of Taiwan (Hymenoptera: Agaonidae: Agaoninae). Journal of the Taiwan Museum, 50, 113-154.

Compton, S. G., Ball, A. D., Collinson, M. E., Hayes, P., Rasnitsyn, A. P., & Ross, A. J. (2010). Ancient fig wasps indicate at least 34 Myr of stasis in their mutualism with fig trees. Biology Letters, 16, 838-842.

Corner, E. J. H. (1958). An introduction to the distribution of Ficus. Reinwardtia, 4, 325-355.

Corner, E. J. H. (1960). Taxonomic notes on Ficus Linn., Asia and Australasia. XI. Subgenus Pharmacosycea Miq. The Gardens’ Bulletin Singapore, 17, 368-485.

Corner, E. J. H. (1967). Ficus in the Solomon Islands and its bearing on the post-Jurassic history of Melanesia. Philosophical Transactions of the Royal Society B, 253, 23-159.

Cook, J. M., Bean, D., Power, S. A., & Dixon, D. J. (2004). Evolution of a complex coevolved trait: active pollination in a genus of fig wasps. Journal of Evolutionary Biology, 17, 238-246.

Cruaud, A., Jabbour-Zahab, R., Genson, R., Cruaud, C., Couloux, A., Kjellberg, F., van Noort, S., & Rasplus, J. Y. (2009). Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approach. Cladistics, 26, 359-387.

Cruaud, A., Jabbour-Zahab, R., Genson, G., Couloxux, A., Yan-Qiong, P., Rong, Y. D., … Rasplus, Y. R. (2011). Out of Australia and back again: the world-wide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae). Journal of Biogeography, 38, 209-225.

Cruaud, A., Rønsted, N., Chantarasuwan, B., Chou, L. S., Clement, W. L., Couloux, A., … Savolainen, V. (2012). An extreme case of plant-insect codiversification: Figs and fig-pollinating wasps. Systematic Biology, 61, 1029-1047.

Datwyler, S. L., & Weiblen, G. D. (2004). On the origin of the fig: Phylogenetic relationships of Moraceae from NDHF sequences. American Journal of Botany, 91, 767-777.

Erasmus, J. C., van Noort, S., Jousselin, E., & Greeff, J. M. (2007). Molecular phylogeny of fig wasps pollinators (Agaonidae, Hymenoptera) of Ficus section Galoglychia. Zoologica Scrypta, 36, 61-78.

Graham, M. V. de V. (1969). The Pteromalidae of North-Western Europe (Hymenoptera: Chalcidoidea). Bulletin of the British Museum (Natural History) (Entomology) Suppl., 16, 1-908.

Grandi, G. (1916). Contributo alla conoscenza degli Agaonini (Hymenoptera, Chalcididae) di Ceylon e dell' India. Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d'Agricoltura, Portici, 11, 183-234.

Harrison, R. D. (2005). Figs and the diversity of tropical rainforest. BioScience, 55, 1053-1064.

Heraty, J. M., Burks, R. A., Cruaud, A., Gibson, G. A. P., Liljeblad, J., Munro, J., … Yoder, M. (2013). A phylogenetic analysis of megadiverse Chalcidoidea (Hymenoptera). Cladistics, 29, 466-542.

Herre, E. A., Machado, C. A., Bermingham, E., Nason, J. D., Windsor, D. M., McCafferty, S. S., … Bachma, K. (1996). Molecular phylogenies of figs and their pollinator wasps. Journal of Biogeography, 23, 521-530.

Iturralde-Vinent, M., & MacPhee, R. (1996). Age and paleogeographic origin of Dominican amber. Science, 273, 2750-2752.

Jiang, Z. F., Huang, D. W., Zhu, C. D., & Zhen, W. Q. (2006). New insights into the phylogeny of fig pollinators using Bayesian analyses. Molecular Phylogenetics and Evolution, 38, 306-315.

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.

Kjellberg, F., Jousselin, E., Bronstein, J. L., Patel, A., Yokoyama, J., & Rasplus, J. Y. (2001). Pollination mode in fig wasps: the predictive power of correlated traits. Proceedings of the Royal Society B, 268, 1113-1121.

Lopez-Vaamonde, C., Dixon, D. J., Cook, J. M., & Rasplus, J. Y. (2002). Revision of the Australian species of Pleistodontes (Hymenoptera: Agaonidae) fig-pollinating wasps and their host-plant associations. Zoological Journal of the Linnean Society, 136, 637-683.

Lopez-Vaamonde, C., Wikström, N., Kjer, K. M., Weiblen, G. D., Rasplus, J. Y., Machado, C. A., & Cook, J. M. (2009). Molecular dating and biogeography of fig-pollinating wasps. Molecular Phylogenetics and Evolution, 52, 715-726.

Machado, C. A., Herre, E. A., McCafferty, S., & Bermingham, E. (1996). Molecular phylogenies of fig pollinating and non-pollinating wasps and the implications for the origin and evolution of the fig-fig wasp mutualism. Journal of Biogeography, 23, 531-542.

Machado, C. A., Jousselin, E., Kjellberg, F., Compton, S. G., & Herre, E. A. (2001). Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proceedings of the Royal Society B, 268, 685-694.

Mayr, G. L. (1885). Feigeninsecten. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien, 35, 147-250.

McKey, D. (1989). Population biology of figs: Applications for conservation. Experientia, 45, 661-673.

Munro, J. B., Heraty, J. M., Burks, R. A., Hawks, D., Mottem, J., Cruaud, A., Rasplus, J. Y., & Jansta, P. (2011). A molecular phylogeny of the Chalcidoidea (Hymenoptera). PLoS ONE, 6(11): e27023.

Murray, M. G. (1985). Figs (Ficus spp.) and fig wasps (Chalcidoidea, Agaonidae): hypotheses for an ancient symbiosis. Biological Journal of the Linnean Society, 26, 69-81.

Peñalver, E., Engel, M. S., & Grimaldi, D. A. (2006). Fig wasps in Dominican amber (Hymenoptera: Agaonidae). American Museum Novitates, 3541, 1-15.

Ramírez, W. (1970). Taxonomic and biological studies of Neotropical fig wasps (Hymenoptera: Agaonidae). The University of Kansas Science Bulletin, 49, 1-44.

Ramírez, W. (1978). Evolution of mechanisms to carry pollen in Agaonidae (Hymenoptera: Chalcidoidea). Tijdschrift voor Entomologie, 121, 279-293.

Ramírez, W. (1989). Dispersal and colonization of Ficus in the New World. In P. R. Crane & S. Blackmore (Eds.), Evolution, Systematics, and Fossil History of the Hamamelidae, ‘Higher’ Hamamelidae’(vol. 2, pp. 279-284). Oxford, UK: Clarendon Press.

Ramírez, W. (1991). Evolution of the mandibular appendage in fig wasps (Hymenoptera: Agaonidae). Revista de Biología Tropical, 39, 87-95.

Ramírez, W. (1994). Hybridization of Ficus religiosa with F. septica and F. aurea (Moraceae). Revista de Biología Tropical, 42, 339-342.

Ramírez, W. (2007). Pollination analogies between Orchidaceae, Ficus (Moraceae) and Asclepiadaceae. Lankesteriana, 7, 450-457.

Ramírez, W., Gómez, J., Salazar, L., & Aguilar, H. (2011). Ficus trigonata (Moraceae) and associated invertebrates organisms living in its syconia in Cocos Island. Costa Rica. Brenesia, 75-76, 16-22.

Ramírez, W., & Malavasi, J. (1997). Fig wasps: mechanisms of pollen transfer in Malvanthera and Pharmacosycea figs (Moraceae). Revista de Biología Tropical, 45, 1635-1640.

Ramírez, W., Monge, J., & Chavarría, J. B. (2009). Sex ratio in two species of Pegoscapus wasps (Hymenoptera: Agaonidae) that develop in figs: can wasps do mathematics, or play sex ratio games. Revista de Biología Tropical, 57, 605-621.

Ramírez, W., & Salazar, L. (2015). Parasitodiplogaster citrinema is an internal necrophagous species of the pollinating fig wasp Pegoscapus tonduzi. Nematology, 17, 733-738.

Rasplus, J. Y., Kerdelhué, C., Le Clainche, I., & Mondor, G. (1998). Molecular phylogeny of fig wasps Agaonidae are not monophyletic. Comptes Rendus de l'Academie des Sciences. Series III, Sciences de la Vie, 321, 517-527.

Rønsted, N., Weiblen, G., Clement, W. L., Zerega, N. J. C., & Savolainen, P. (2008). Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis, 45, 45-55.

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, 272, 2593-2599.

Saunders, S. S. (1883). Descriptions of three new genera and species of fig insects allied to Blastophaga from Calcutta, Australia, and Madagascar; with notes on their parasites and of the affinities of the respective races. Transactions of the Royal Entomological Society of London, 31, 1-28.

Segar, S. T., Lopez-Vaamonde, C., Rasplus, J. Y., & Cook, J. M. (2012). The global phylogeny of the subfamily Sycoryctinae (Pteromalidae): parasites of an obligate mutualism. Molecular Phylogenetics and Evolution, 65, 116-125.

Wang, G., Chen, J., Li, Z. B., Zhang, F. P., & Yang, D. R. (2014). Has pollination mode shaped the evolution of Ficus pollen? PLoS ONE, 9(1), E86231. doi 10.1371/journal.pone.0086231

Weiblen, G. D. (2000). Phylogenetic relationships of functionally dioecious Ficus (Moraceae) based on ribosomal DNA sequences and morphology. American Journal of Botany, 87, 1342-1357.

Weiblen, G. D. (2002). How to be a fig wasp. Annual Review of Entomology, 47, 299-330.

Wiebes, J. T (1977). Zoologische Mededelingen Uitgegeven Door Het. Indo-Malayan and Papuan fig Wasps (Hymenoptera, Chalcidoidea) 7. Agaonidae, mainly caught at light, 52, 136-159.

Wiebes, J. T (1979). The fig wasps genus Dolichoris Hill (Hymenoptera Chalcidoidea, Agaonidae). Proceedings. Koninklijke Nederlandse Akademie van Wetenschappen, Amsterdam (C), 82, 181-196.

Wiebes, J. T. (1982). The phylogeny of the Agaonidae (Hymenoptera, Chalcidoidea). Netherlands Journal of Zoology, 32, 395-411.

Wiebes, J. T. (1995). The New World Agaoninae (pollinators of figs) (Vol. 94, pp. 1-60). Amsterdam, North-Holland.

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.

Zerega, N. J., Clement, W. L., Datwyler, S. L., & Weiblen, G. D. (2005). Biogeography and divergence times in the mulberry family (Moraceae). Molecular Phylogenetics and Evolution, 37, 402-406.

Comments

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright (c) 2016 Revista de Biología Tropical

Downloads

Download data is not yet available.