Evolutionary relationships among pollinators and repeated pollinator sharing in sexually deceptive orchids

Abstract

The mechanism of pollinator attraction is predicted to strongly influence both plant diversification and the extent of pollinator sharing between species. Sexually deceptive orchids rely on mimicry of species-specific sex pheromones to attract their insect pollinators. Given that sex pheromones tend to be conserved among related species, we predicted that in sexually deceptive orchids, (i) pollinator sharing is rare, (ii) closely related orchids use closely related pollinators and (iii) there is strong bias in the wasp lineages exploited by orchids. We focused on species that are pollinated by sexual deception of thynnine wasps in the distantly related genera Caladenia and Drakaea, including new field observations for 45 species of Caladenia. Specialization was extreme with most orchids using a single pollinator species. Unexpectedly, seven cases of pollinator sharing were found, including two between Caladenia and Drakaea, which exhibit strikingly different floral morphology. Phylogenetic analysis of pollinators using four nuclear sequence loci demonstrated that although orchids within major clades primarily use closely related pollinator species, up to 17% of orchids within these clades are pollinated by a member of a phylogenetically distant wasp genus. Further, compared to the total diversity of thynnine wasps within the study region, orchids show a strong bias towards exploiting certain genera. Although these patterns may arise through conservatism in the chemical classes used in sex pheromones, apparent switches between wasp clades suggest unexpected flexibility in floral semiochemical production. Alternatively, wasp sex pheromones within lineages may exhibit greater chemical diversity than currently appreciated.

(Methylthio)phenol semiochemicals are exploited by deceptive orchids as sexual attractants for Campylothynnus thynnine wasps

“…Prior to our discovery of pollination by Campylothynnus sp. A [6], it was thought that C. attingens subsp. attingens was pollinated solely by sexual deception of an undescribed species of Thynnoides [6].…”

“…This strategy is known from over 20 genera of orchids, with all cases studied thus far confirmed to use chemicals for long-distance attraction of pollinators [2]. As a by-product of mimicking the highly specific sex pheromone systems of insects, these orchids are highly specialised, typically with a single predominant pollinator species [3][4][5][6]. With multiple origins of sexual deception, Australia is a centre of diversity for this pollination strategy, with more than 100 orchid species spanning at least 11 genera exploiting either male Hymenoptera (ants, ichneumonid wasps, scoliid wasps, thynnine wasps, and sawflies) or male Diptera (fungus gnats) ( [2,5,7].…”

“…This genus appears to be unique among orchid genera in that it includes examples of orchids that achieve pollination by either rewarding, food deceptive or sexually deceptive strategies [18][19][20]. Nonetheless, pollination by sexual deception dominates within Caladenia, with at least 200 species predicted to use this pollination strategy [6,19,21]. Furthermore, these sexually deceptive species exploit male thynnine wasps as pollinators drawn from across at least 34 wasp genera [6,19], suggesting the potential for a wide diversity of semiochemical systems.…”

“…Nonetheless, pollination by sexual deception dominates within Caladenia, with at least 200 species predicted to use this pollination strategy [6,19,21]. Furthermore, these sexually deceptive species exploit male thynnine wasps as pollinators drawn from across at least 34 wasp genera [6,19], suggesting the potential for a wide diversity of semiochemical systems. In this study, we extend our investigations into the chemical ecology of sexual deception in Caladenia.…”

Does size really matter? A comparative study on floral traits in orchids with two different pollination strategies

“…In angiosperms, a large specialisation of floral traits is often associated with a dominance of prezygotic barriers compared to postzygotic barriers, where their co‐occurrence leads to the maintenance of species boundaries (Darwin ; Phillips et al . ). Although a highly specialised pollination strategy allows benefits and a reduction in pollen loss, it also has different negative side effects, such as an increasing risk of extinction (Waser ).…”