Convergent evolution of floral signals underlies the success of Neotropical orchids

Abstract

The great majority of plant species in the tropics require animals to achieve pollination, but the exact role of floral signals in attraction of animal pollinators is often debated. Many plants provide a floral reward to attract a guild of pollinators, and it has been proposed that floral signals of non-rewarding species may converge on those of rewarding species to exploit the relationship of the latter with their pollinators. In the orchid family (Orchidaceae), pollination is almost universally animal-mediated, but a third of species provide no floral reward, which suggests that deceptive pollination mechanisms are prevalent. Here, we examine floral colour and shape convergence in Neotropical plant communities, focusing on certain food-deceptive Oncidiinae orchids (e.g. Trichocentrum ascendens and Oncidium nebulosum) and rewarding species of Malpighiaceae. We show that the species from these two distantly related families are often more similar in floral colour and shape than expected by chance and propose that a system of multifarious floral mimicry--a form of Batesian mimicry that involves multiple models and is more complex than a simple one model-one mimic system--operates in these orchids. The same mimetic pollination system has evolved at least 14 times within the species-rich Oncidiinae throughout the Neotropics. These results help explain the extraordinary diversification of Neotropical orchids and highlight the complexity of plant-animal interactions.

Keywords: Neotropical plant communities; Oncidiinae; convergent evolution; deceptive pollination; insect colour vision.

Figure 1.

Floral resemblance of Stigmaphyllon sp. (centre; Malpighiaceae) and Oncidiinae orchids Trichocentrum ascendens and Rossioglossum ampliatum (left and right; Oncidiinae: Orchidaceae).

Figure 2.

Bee-UV-green Oncidiinae (open circles) and Malpighiaceae species (open triangles) occupy a different portion of bee colour space when compared with the majority of other local flowering species (blue diamonds). Non-bee-UV-green orchids are represented by open squares. Colour loci are calculated according to the hexagon colour model of hymenopteran vision [41]. The inset shows the colour hexagon divided into sections that represent colour names as termed with respect to insect vision (B, blue; G, green; UV, ultraviolet), indicating relative contributions from individual colour receptor types of hymenoptera.

Figure 3.

Convergence on a shared area in bee colour space has evolved and been lost multiple times within Oncidiinae. Reproductive strategy, bee-UV-green coloured flowers (black branches) or non-bee-UV-green flowers (white branches), mapped onto the phylogenetic tree of the Oncidiinae. The majority of nodes are well supported (see the electronic supplementary material for details) and agree well with results of Neubig et al. [28], who included more taxa and a larger number of DNA regions. Letters in brackets beside the clade name represent the 10 major clades in Oncidiinae [27].

Figure 4.

(a) Eigenshape (ES) morphometric analysis of Costa Rican angiosperms. Each point represents the position of an individual species in shape space (Malpighiaceae in blue, yellow-flowered Oncidiinae in red and all other angiosperms in green); (b) Eigenshape analysis of Oncidiinae labellum shape. Each blue pin represents a yellow-flowered species and each red pin a non-yellow-flowered species.