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.2012 Oct;99(10):1666-79.
doi: 10.3732/ajb.1200274. Epub 2012 Sep 10.

Reconstructing the origin and elaboration of insect-trapping inflorescences in the Araceae

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Reconstructing the origin and elaboration of insect-trapping inflorescences in the Araceae

David Bröderbauer et al. Am J Bot.2012 Oct.

Abstract

Premise of the study: Floral traps are among the most sophisticated devices that have evolved in angiosperms in the context of pollination, but the evolution of trap pollination has not yet been studied in a phylogenetic context. We aim to determine the evolutionary history of morphological traits that facilitate trap pollination and to elucidate the impact of pollinators on the evolution of inflorescence traps in the family Araceae. •

Methods: Inflorescence morphology was investigated to determine the presence of trapping devices and to classify functional types of traps. We inferred phylogenetic relationships in the family using maximum likelihood and Bayesian methods. Character evolution of trapping devices, trap types, and pollinator types was then assessed with maximum parsimony and Bayesian methods. We also tested for an association of trap pollination with specific pollinator types. •

Key results: Inflorescence traps have evolved independently at least 10 times within the Araceae. Trapping devices were found in 27 genera. On the basis of different combinations of trapping devices, six functional types of traps were identified. Trap pollination in Araceae is correlated with pollination by flies. •

Conclusions: Trap pollination in the Araceae is more common than was previously thought. Preadaptations such as papillate cells or elongated sterile flowers facilitated the evolution of inflorescence traps. In some clades, imperfect traps served as a precursor for the evolution of more elaborate traps. Traps that evolved in association with fly pollination were most probably derived from mutualistic ancestors, offering a brood-site to their pollinators.

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Figures

Fig. 1
Fig. 1
Inflorescence morphology of selected Araceae. (A)Anthurium digitatum (Jacq.) Schott, spadix with bisexual flowers and an expanded spathe. (B)Arum nigrum Schott, spadix with unisexual and sterile flowers and a spathe separated into a tube and a blade. The front part of the spathe tube is removed for better visibility of the spadix; a = pistillate flowers; b = elongated sterile flowers; c = staminate flowers; d = sterile appendix. Scale bars = 1 cm.
Fig. 2
Fig. 2
Ancestral state reconstructions of trap pollination in Araceae. Colors on lines indicate reconstruction of trap types (A) with maximum parsimony in Mesquite 2.0. In cases where lines have more than one color, ancestral states could not be resolved unambiguously. Pie charts on the nodes display the posterior probabilites of trap types calculated with Bayesian inference in SIMMAP 1.5. Pie charts below the nodes display the posterior probabilites of pollinator types (B). Arrows point at the earliest appearance of the four types of spathe shape (C). Bars indicate the appearance of characters D-G along the phylogeny. Coding for all characters is shown at the right. Node numbers are referred to in the text.
Fig. 3
Fig. 3
Slippery surfaces on the adaxial spathe epidermis in Araceae. (A) Wax platelets (Steudnera kerrii Gagnep.). (B) Wax tubules and threads (Amorphophallus taurostigma Ittenbach, Hett. & Bogner). (C) Imbricate downward pointing papillate cells and branched wax rodlets [Urospatha sagittifolia (Rudge) Schott]. (D) Downward pointing papillate cells (Helicodiceros muscivorus L.f.). (E) Imbricate downward-pointing papillate cells with cuticular folds (Dracontium asperum K. Koch). (F) Wax platelets on perpendicular papillate cells (Stylochaeton cf.hypogaeus Lepr.).Note: Cells in samples A–C and F have shrunk due to drying at room temperature. Scale bars = 10 µm.
Fig. 4
Fig. 4
Spathe closure during anthesis. (A–C)Colocasia fontanesii Schott. (A) The spathe blade opens a narrow slit (arrowhead) during the pistillate phase. (B) The spathe blade closes at the end of the pistillate phase. (C) The spathe blade reopens and reflexes during the staminate phase. The constriction above the spathe chamber is now closed. (D–F)Typhonium trilobatum (L.) Schott. (D) The spathe constriction above the floral chamber opens at the beginning of the pistillate phase and spadix tilts forward. (E) The constriction closes at the end of the pistillate phase; the spadix is erect. The color of the spathe blade gradually turns from red to brown. (F) The constriction reopens during the staminate phase, and the spadix tilts forward again. Scale bars = 1 cm.
Fig. 5
Fig. 5
Functional types of traps in Araceae. (A)Schismatoglottis type. The insects are retained by spathe movements; slippery surfaces are absent. (B)Arisarum type. An imperfect trap with a slippery spathe surface. Insects slip and fall into the spathe chamber but can escape unhampered by climbing the spadix or flying off. (C)Zomicarpa type. Insects are trapped inside the inflorescence by slippery surfaces and are released through a secondary exit formed by a movement of the spathe. (D)Typhonium type. Insects glide down slippery surfaces and are retained in the floral chamber by closure of the spathe constriction. During the staminate phase, the constriction reopens, and slippery surfaces cease to be slippery. (E)Arum type. The insects are trapped by slippery spathe surfaces and sterile flowers on the spadix that partially occlude the spathe chamber. Insect release is facilitated by withering of the slippery organs. (F)Stylochaeton type. Insects are trapped by slippery spathe surfaces. In the pistillate phase, the spadix is enclosed in the spathe chamber. During the staminate phase, the spadix grows out of the chamber, and insects can escape via climbing. Gender symbols indicate pistillate and staminate phase of anthesis. Black arrows indicate arrival and departure of pollinators. Arrowheads indicate closure of the spathe constriction. The insect symbol indicates the pollinator’s residence during arrest. Asterisks indicate the presence of an intact slippery surface; crosses indicate that the slippery surface has withered and ceased to be functional.
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