Exploitation of an ancestral pheromone biosynthetic pathway contributes to diversification in Heliconius butterflies

Abstract

During courtship, male butterflies of many species produce androconial secretions containing male sex pheromones (MSPs) that communicate species identity and affect female choice. MSPs are thus likely candidates as reproductive barriers, yet their role in speciation remains poorly studied. Although Heliconius butterflies are a model system in speciation, their MSPs have not been investigated from a macroevolutionary perspective. We use GC/MS to characterize male androconial secretions in 33 of the 69 species in the Heliconiini tribe. We found these blends to be species-specific, consistent with a role in reproductive isolation. We detected a burst in blend diversification rate at the most speciose genus, Heliconius; a consequence of Heliconius and Eueides species using a fatty acid (FA) metabolic pathway to unlock more complex blends than basal Heliconiini species, whose secretions are dominated by plant-like metabolites. A comparison of 10 sister species pairs demonstrates a striking positive correlation between blend dissimilarity and range overlap, consistent with character displacement or reinforcement in sympatry. These results demonstrate for the first time that MSP diversification can promote reproductive isolation across this group of butterflies, showcasing how implementation of an ancestral trait, the co-option of the FA metabolic pathway for pheromone production, can facilitate rapid speciation.

Keywords: chemical ecology; macroevolution; reproductive isolation; sympatric speciation.

Figure 1.

Heliconiini tree with branches coloured according to disparity in pheromone profiles. Values for disparity (expressed by Euclidean distance) are shown at each node. The table shows putative MSPs composition (Dataset C) of each species, where columns represent androconia-exclusive compounds and amounts are expressed as the proportion of the total androconial contents. Note the near absence FA derivatives among the basal genera, while in general Eueides and Heliconius species produce a varied cocktail comprising both plant-like metabolites and FA derivatives. This figure summarizes the most abundant compounds (at least 12% of the total androconial contents). For a complete dataset with all compounds, see (electronic supplementary material, table S6). (Online version in colour.)

Figure 2.

Relationship between dissimilarity in MSPs (Euclidean distance) and range overlap between Heliconiini sister species pairs. Divergence time between each sister species pair is represented as a logged colour scale. Each point is a pair of sister species: AH, H. atthis–H. hecale; BW, H. burneyi–H. wallacei; CP, H. cydno–H. pachinus; CT, H. clysonimus–H. telesiphe; DD, Dryas iulia–Dryadula phaetusa; EE, Eueides tales–Eueides lybia; EH, H. erato–H. himera; EP, H. elevatus–H. pardalinus; HX, H. hierax–H. xanthocles; IN, H. ismenius–H. numata. (Online version in colour.)