A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies

Abstract

Plants and insects often use the same compounds for chemical communication, but not much is known about the genetics of convergent evolution of chemical signals. The terpene (E)-β-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. While the biosynthesis of terpenes has been described in plants and microorganisms, few terpene synthases (TPSs) have been identified in insects. Here, we study the recent divergence of 2 species, H. melpomene and Heliconius cydno, which differ in the presence of (E)-β-ocimene; combining linkage mapping, gene expression, and functional analyses, we identify 2 novel TPSs. Furthermore, we demonstrate that one, HmelOS, is able to synthesise (E)-β-ocimene in vitro. We find no evidence for TPS activity in HcydOS (HmelOS ortholog of H. cydno), suggesting that the loss of (E)-β-ocimene in this species is the result of coding, not regulatory, differences. The TPS enzymes we discovered are unrelated to previously described plant and insect TPSs, demonstrating that chemical convergence has independent evolutionary origins.

Identification and Composition of Clasper Scent Gland Components of the Butterfly Heliconius erato and Its Relation to Mimicry

“…Terpene elongation can of course also take place by other enzymes, e. g. decaprenyl synthases also known from Heliconius. [16] The biosynthesis of the major CSG terpenes can be explained as shown in Figure 10. A pyrophosphate precursor of different chain length can be transformed into terpene hydrocarbons of the αor β-farnesene type.…”

Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae)

“…Additionally, multiple male traits as a mechanism aiding reproductive isolation might become less important if closely related species discriminate between the chemical signals produced by these androconia. For instance, Heliconius butterflies do not vary significantly in their number of androconial organs; however, there is striking betweenspecies variation in chemical bouquets [57,58]. These chemical blends drive female preference for conspecific males in sympatric, co-mimetic species, and seem to evolve rapidly with pheromone gains and losses occurring frequently across the Heliconius phylogeny [58][59][60].…”

“…For instance, Heliconius butterflies do not vary significantly in their number of androconial organs; however, there is striking betweenspecies variation in chemical bouquets [57,58]. These chemical blends drive female preference for conspecific males in sympatric, co-mimetic species, and seem to evolve rapidly with pheromone gains and losses occurring frequently across the Heliconius phylogeny [58][59][60]. Hence, rapid divergent chemical evolution might render the loss of multiple secondary sexual characters more likely.…”

Small molecules as products of evolution

“…The importance of convergence to reveal basic principles of the evolution of small molecules (such as catalytic promiscuity) is also well exemplifi ed by a pheromone system involved in relationships between butterfl ies and plants. It has long been known that plants and insects often use the same compounds for communication, and now the underlying biochemical mechanisms are starting to be uncovered 17 . Even within plants, there are multiple examples of convergent evolution, with promiscuous cytochrome p450s (CYPs) being recruited many times into identical catalytic reactions, either among closely related subfamilies, or even across most distant paralogs 18 .…”