Convergent evolution of sexual deception via chromatic and achromatic contrast rather than colour mimicry

Abstract

The Orchidaceae is characterised by the repeated evolution of sexual deception, one of the most specialised pollination strategies. In orchids, sexual deception involves long-range pollinator attraction via mimicry of female insect sex pheromones. At close range, visual signals involving colour mimicry, contrast to the background, and exploitation of pollinator sensory biases could attract pollinators, but remain largely untested. Here we focus on a remarkable system in which species from two only distantly related sexually deceptive orchid genera with strikingly different flowers (Drakaea livida and three species of Caladenia) share the same pollinator, males of the thynnine wasp Zaspilothynnus nigripes. We used spectral reflectance measurements and modelling to investigate pollinator perception of colour, including the first examination of overall colour patterns in flowers via colour pattern geometry analyses. Rather than closely matching the colours of female Z. nigripes, these orchids had strong chromatic and achromatic contrast against their backgrounds. For Caladenia, the sepals and petals show high contrast, while in D. livida, which has diminutive petals and sepals, it is the labellum that contrasts strongly against the background. Despite varying in colour, the Caladenia species all had strong within-flower contrast between a UV-bright central target (column and labellum) and a corolla of radiating stripes (petals and sepals). The colour pattern geometry analyses also indicated that the orchids’ overall colour patterns are highly conspicuous against their backgrounds. Contrast, UV, and target patterns could all enhance detection, and exploit pollinators’ innate preferences. Since colour contrast may function with a range of colours and floral forms, attracting pollinators via contrast rather than visual mimicry may be a critical but previously overlooked process facilitating the evolution of sexual deception.