Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: Implications for pollinator-driven speciation

•Sexually deceptive orchids are predicted to represent a special case of plant speciation where strong reproductive isolation may be achieved by differences in floral scent. •In this study of Australian sexually deceptive Chiloglottis orchids, we performed choice experiments to test for wasp pollinator specificity in the field; identified the compounds involved in pollinator attraction by gas chromatography with electroantennographic detection (GC-EAD), gas chromatography with mass selective detection (GC-MS), chemical synthesis and behavioural bioassays; and mapped our chemical findings on to a phylogeny of the orchids. •Field experiments confirmed pollination is a highly specific interaction, but also revealed a pool of nonpollinating 'minor responder' wasps. Six novel compounds, all 2,5-dialkylcyclohexan-1,3-diones, called 'chiloglottones', were discovered to be involved in pollinator attraction. Bioassays confirmed that pollinator specificity has a strong chemical basis, with specificity among sympatric orchids maintained by either different single compounds or a variation in a blend of two compounds. The phylogenetic overlay confirmed that speciation is always associated with pollinator switching and usually underpinned by chemical change. •If the chemical differences that control reproductive isolation in Chiloglottis have a strong genetic basis, and given the confirmed pool of potential pollinators, we conclude that pollinator-driven speciation appears highly plausible in this system.