Amino Acid Change in an Orchid Desaturase Enables Mimicry of the Pollinator's Sex Pheromone

Mimicry illustrates the power of selection to produce phenotypic convergence in biology [1]. A striking example is the imitation of female insects by plants that are pollinated by sexual deception of males of the same insect species [2 3 and 4]. This involves mimicry of visual tactile and chemical signals of females [2 3 4 5 6 and 7] especially their sex pheromones [8 9 10 and 11]. The Mediterranean orchid Ophrys exaltata employs chemical mimicry of cuticular hydrocarbons particularly the 7 alkenes in an insect sex pheromone to attract and elicit mating behavior in its pollinators males of the cellophane bee Colletes cunicularius [ 11 12 and 13]. A difference in alkene double bond positions is responsible for reproductive isolation between O. exaltata and closely related species such as O. sphegodes [ 13 14 15 and 16]. We show that these 7 alkenes are likely determined by the action of the stearoyl acyl carrier protein desaturase (SAD) homolog SAD5. After gene duplication changes in subcellular localization relative to the ancestral housekeeping desaturase may have allowed proto SAD5’s reaction products to undergo further biosynthesis to both 7 and 9 alkenes. Such ancestral coproduction of two alkene classes may have led to pollinator mediated deleterious pleiotropy. Despite possible evolutionary intermediates with reduced activity amino acid changes at the bottom of the substrate binding cavity have conferred enzyme specificity for 7 alkene biosynthesis by preventing the binding of longer chained fatty acid (FA) precursors by the enzyme. This change in desaturase function enabled the orchid to perfect its chemical mimicry of pollinator sex pheromones by escape from deleterious pleiotropy supporting a role of pleiotropy in determining the possible trajectories of adaptive evolution.