Abstract
Sexually deceptive orchids lure pollinators by mimicking female insects. Male insects fooled into gripping or copulating with orchids unwittingly transfer the pollinia. The effect of deception on pollinators has been considered negligible, but we show that pollinators may suffer considerable costs. Insects pollinating Australian tongue orchids (Cryptostylis species) frequently ejaculate and waste copious sperm. The costs of sperm wastage could select for pollinator avoidance of orchids, thereby driving and maintaining sexual deception via antagonistic coevolution or an arms race between pollinator learning and escalating orchid mimicry. However, we also show that orchid species provoking such extreme pollinator behavior have the highest pollination success. How can deception persist, given the costs to pollinators? Sexually-deceptive-orchid pollinators are almost exclusively solitary and haplodiploid species. Therefore, female insects deprived of matings by orchid deception could still produce male offspring, which may even enhance orchid pollination.
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