The evolution of floral deception in Epipactis veratrifolia (Orchidaceae): From indirect defense to pollination

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Abstract

Background: It is estimated that floral deception has evolved in at least 7500 species of angiosperms, of which two thirds are orchids. Epipactis veratrifolia (Orchidaceae) is a model system of aphid mimicry as aphidophagous hoverflies lay eggs on false brood sites on their flowers. To understand the evolutionary ecology of floral deception, we investigated the pollination biology of E. veratrifolia across 10 populations in the Eastern Himalayas. We reconstructed the phylogeny of Epipactis and mapped the known pollination systems of previously studied species onto the tree.Results: Some inflorescences of E. veratrifolia were so infested with aphids while they were still in bud that the some larvae of hoverflies developed to the third instar while flower buds opened. This indicated that adult female hoverflies were partly rewarded for oviposition. Although flowers failed to secrete nectar, they mimicked both alarm pheromones and aphid coloring of to attract female hoverflies as their exclusive pollinators. Phylogenetic mapping indicate that pollination by aphidophagous hoverflies is likely an ancestral condition in the genus Epipactis. We suggest that the biological interaction of aphid (prey), orchid (primary producer) and hoverfly (predator) may represent an intermediate stage between mutualism and deception in the evolution of pollination-by-deceit in E. veratrifolia.Conclusions: Our analyses indicate that this intermediate stage may be used as a model system to interpret the origin of oviposition (brood site) mimicry in Epipactis. We propose the hypothesis that some deceptive pollination systems evolved directly from earlier (partly) mutualistic systems that maintained the fidelity of the original pollinator(s) even though rewards (nectar/ brood site) were lost. © 2014 Jin et al.; licensee BioMed Central Ltd.

Figures

  • Figure 1 Aphids hoverflies (adults and maggots) on buds and flowers. (A) A hoverfly on a flower transporting the pollinaria on its dorsal thorax (arrow indicates position of pollinia). (B) Hoverfly carrying pollinia while laying an egg on a flower (arrow indicates the egg). (C) Aphids on inflorescences flowering in March (arrows indicate aphids and a hoverfly egg). (D) A second instar maggot preying on aphids on a flower (arrows indicate hoverfly instar and anther cap). Scale interpretation: A and B, average length of hoverfly = 9–10 mm; C, average length of aphids = 1 mm; D, average length of anther cap = 3 mm.
  • Figure 2 Percentage of inflorescences with hoverfly eggs. (A) The percentage of inflorescences in bud in March bearing eggs. (B) The percentage of inflorescence with open flowers in March bearing eggs. (C) The percentage of inflorescences with open flowers in April bearing eggs.
  • Table 1 Breeding system of Epipactis veratrifolia in 2011
  • Table 2 Natural fruit produced by Epipactis veratrifolia in 201
  • Figure 3 GC-MS traces of (A) headspace volatiles of the flower of Epipactis veratrifolia; (B) surface extract of specimens of Aulacorthum solani.
  • Figure 4 The reflectance of aphids and anther caps. (A) Reflectance of aphids, two lines representing two replicates, each on a group of aphids.
  • Figure 5 Phylogeny and evolutionary pattern of pollination system of Epipactis. (A) Phylogram of the Epipactis lineage. (B) Mapping of pollination systems in Epipactis onto the phylogram. Numbers at the nodes are Bayesian posterior probabilities and bootstrap percentages (>50%).
  • Table 3 Intraspecific variation in the pollination characteristics of E. veratrifoliain the Eastern Himalayas and Israel (Ivri & Dafni, 1977). + = character present; - = character absent

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Jin, X. H., Ren, Z. X., Xu, S. Z., Wang, H., Li, D. Z., & Li, Z. Y. (2014). The evolution of floral deception in Epipactis veratrifolia (Orchidaceae): From indirect defense to pollination. BMC Plant Biology, 14(1). https://doi.org/10.1186/1471-2229-14-63

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