Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptiveChiloglottisorchids: implications for pollinator‐driven speciation

Abstract

Summary 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.

Floral trait variation and integration as a function of sexual deception in Gorteria diffusa

“…Pollination by sexual deception is most prevalent in the Orchidaceae, and commonly in these sexually deceptive orchids, pollinator attraction has a significant olfactory component, including pheromone mimicry [25,26]. However, more recently a parallel system of sexual deception has emerged outside of the Orchidaceae, in Gorteria diffusa Thunb.…”

Floral scent and species divergence in a pair of sexually deceptive orchids

“…Our finding of higher proportions of two alkenes and wax esters in O. aymoninii is in agreement with early investigations (Borg‐Karlson, Groth, Ågren, & Kullenberg, 1993) that also detected higher amounts of esters in O. aymoninii plants compared to O. insectifera . We show here that two esters and alkenes are sufficient to increase the attractiveness toward another pollinator significantly; this suggests that whereas Ophrys species typically differ in a range of scent components, key differences for specific pollinator attraction may be less complex, even reminiscent of the chemical simplicity in Australian genus Chiloglottis , where differences in single compounds are sufficient to trigger pollinator switches (Peakall et al., 2010). …”

“…As yet we do not know, however, whether elevated alkenes/esters also reduce the attraction of the pollinator of O. insectifera , which is a necessary prerequisite for isolation against backcrossing into wild‐type O. insectifera . In previous experiments in sexual mimics of the genus Ophrys and Chiloglottis , however, it has been shown that hetero‐specific scent clearly reduces pollinator attraction (Peakall et al., 2010; Xu, Schlüter, & Schiestl, 2012). Nevertheless, some overlap in pollinators is likely during the switching phase, unless antagonistic pleiotropy between attractive scent compounds would prevent a phenotype emitting a blend of both.…”

Absence of nectar resource partitioning in a community of parasitoid wasps

“…However, some species appear to regularly forage for nectar (Brown and Phillips 2014), where they may also be important pollinators. While over 600 species have been described, ongoing taxonomic and pollination studies have revealed an immense diversity of undescribed taxa at both the species and generic level (Brown 2009;Peakall et al 2010;Griffiths et al 2011;Menz et al 2015). Further, observations of aggregations of mating pairs on nectar plants have shown a high diversity of co-occurring species (Alcock 1981;Phillips et al 2009).…”