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

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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.

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Acknowledgments

ACG thanks those who provided childcare essential for the completion of the analyses and manuscript: Greg Holwell, Val Gaskett, Rika Gaskett and Terry and Ian Holwell. Orchids and wasps were collected under permits from the Department of Parks and Wildlife, Western Australia. We thank John Rudolph for macros for preparing spectral data for analyses and Vivian Ward for the botanical diagrams. Funding for fieldwork and equipment was from a University of Auckland FRDF Grant to ACG and an Australian Orchid Foundation Grant to RDP. The project was completed while RDP was supported by an ARC Linkage Grant (LP110100408) to Rod Peakall, Kingsley Dixon and Celeste Linde and a Discovery Early Career Research Award (DE150101720) and ACG was supported by University of Auckland sabbatical and parental leave funding.

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Online supplementary Fig. 1

Achromatic contrast between sexually deceptive orchids and female wasps of the pollinator species, Zaspilothynnus nigripes. Units are Just Noticeable Differences (JNDs; according to Vorobyev & Osorio 1998). (JPEG 743 kb)

Online supplementary Fig. 2

Contrast between sexually deceptive orchids and male wasps of the pollinator species Zaspilothynnus nigripes for a) chromatic, b) achromatic JNDs. (JPEG 1417 kb)

Online supplementary Fig. 3

Colour contrast between female and male wasps of the sexually deceptive orchid pollinator species, Zaspilothynnus nigripes for a) chromatic, b) achromatic JNDs. (JPEG 809 kb)

Online supplementary Fig. 4

Achromatic contrast between the floral parts within each sexually deceptive orchid species. (JPEG 903 kb)

Online supplementary Fig. 5

Achromatic contrast between sexually deceptive orchids and their substrates. (JPEG 935 kb)

Online supplementary Fig. 6

Achromatic contrast between female wasps of Zaspilothynnus nigripes and substrates of sexually deceptive orchids. (JPEG 526 kb)

Supplementary material 7 (DOCX 13 kb)

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Gaskett, A.C., Endler, J.A. & Phillips, R.D. Convergent evolution of sexual deception via chromatic and achromatic contrast rather than colour mimicry. Evol Ecol 31, 205–227 (2017). https://doi.org/10.1007/s10682-016-9863-2

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