Abstract
Floral innovations are key for pollinator specialization and play a significant role in plant diversification. Orchidaceae present many examples of floral innovations that allow its high degrees of pollinator specialization and promoted speciation. The rich neotropical genus Telipogon evolved an uncinate (=hook-like) viscidium on the pollinarium and setae-bearing flowers, which are uncommon in Orchidaceae; however, the importance of them on pollination success and whether they are floral innovations or exaptations in Telipogon have not been investigated. Here we investigate the morphology of the viscidium and floral setae within the Telipogon alliance (including the genera Hofmeisterella, Trichoceros and Telipogon), test their significance in pollination, and their occurrence and evolution across the Oncidiinae. We used Telipogon peruvianus as a model species to test whether uncinate viscidium and floral setae increased pollination success compared with a cochleariform (=spoon-like) viscidium and lack of floral setae condition. We show that the uncinate viscidium is a synapomorphy for Telipogon; setae-bearing flowers are not universally found among all species of Telipogon and evolved once in the Telipogon alliance. Furthermore, Telipogon peruvianus flowers with an uncinate viscidium have achieved higher pollinia export than those with cochleariform viscidium (ancestral condition), whereas flowers with setae have both higher success in pollinia removal, although not significant, and pollinia deposition than those lacking of setae (ancestral condition). We demonstrate that uncinate viscidia and floral setae in Telipogon are a key innovation and exaptation, respectively, that enhance pollination success and they might act as drivers of diversification and pollinator specialization in this genus.
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Data availability
The sequences analysed during the current study are available in the Dryad digital repository (https://datadryad.org/stash/dataset/doi:10.5061/dryad.2rk39). All the other data generated and analysed during this study are included in this published article (and its supplementary information files).
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Acknowledgements
Abigail Dextre kindly assisted us during fieldwork. Juana and José Gutierrez hosted us in Marcapata town during fieldwork. Benjamin Collantes (Inka-Terra Association) took the pictures of Fig. 4. We thank two anonymous that reviewers provided helpful comments on an earlier version of the manuscript. C.M. thanks to Pedro Romero and Ernesto Razuri for comments on parts of this manuscript. The phylogenetic portion of this study would not have been possible without the dedication, knowledge and mentorship of the late W. Mark Whitten, to whom we dedicated this article.
Funding
The study was supported by the German Academic Exchange Service (DAAD) through a PhD. scholarship to C.M. and the National Geographic through a research grant to M.A and C.M. DNA data were produced with the support of NSF grants DEB-9815821, DEB-9509071, DEB-0234064, and IOB-0543659, by grants from the American Orchid Society Fund for Education and Research, the Florida Museum of Natural History, and the Royal Botanic Gardens, Kew.
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C.M. and M.A. planned the research; C.M. designed the research, collected bibliographic data, conducted lab work and fieldwork, and performed experiments; K.M.N. and N.H.W. collected genetic data; C.M. analysed data and wrote the original draft; C.M., K.M.N., N.H.W. and M.A. reviewed and edited the manuscript.
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Martel, C., Neubig, K.M., Williams, N.H. et al. The uncinate viscidium and floral setae, an evolutionary innovation and exaptation to increase pollination success in the Telipogon alliance (Orchidaceae: Oncidiinae). Org Divers Evol 20, 537–550 (2020). https://doi.org/10.1007/s13127-020-00457-w
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DOI: https://doi.org/10.1007/s13127-020-00457-w