A major locus controls a biologically active pheromone component inHeliconius melpomene

Abstract

Understanding the production, response, and genetics of signals used in mate choice can inform our understanding of the evolution of both intraspecific mate choice and reproductive isolation. Sex pheromones are important for courtship and mate choice in many insects, but we know relatively little of their role in butterflies. The butterfly Heliconius melpomene uses a complex blend of wing androconial compounds during courtship. Electroantennography in H. melpomene and its close relative Heliconius cydno showed that responses to androconial extracts were not species specific. Females of both species responded equally strongly to extracts of both species, suggesting conservation of peripheral nervous system elements across the two species. Individual blend components provoked little to no response, with the exception of octadecanal, a major component of the H. melpomene blend. Supplementing octadecanal on the wings of octadecanal-rich H. melpomene males led to an increase in the time until mating, demonstrating the bioactivity of octadecanal in Heliconius. Using quantitative trait locus (QTL) mapping, we identified a single locus on chromosome 20 responsible for 41% of the parental species' difference in octadecanal production. This QTL does not overlap with any of the major wing color or mate choice loci, nor does it overlap with known regions of elevated or reduced F ST . A set of 16 candidate fatty acid biosynthesis genes lies underneath the QTL. Pheromones in Heliconius carry information relevant for mate choice and are under simple genetic control, suggesting they could be important during speciation. K E Y W O R D S : Behavior, electroantennography, Heliconius, pheromones, quantitative trait locus mapping.

Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies

“…A previous QTL analysis in crosses between H. melpomene and H. cydno found no genetic linkage among colour pattern and/or colour preference loci with the locus underlying the production of octadecanal [71]. This is unexpected if chemical cues play a major role in reproductive isolation, as theory predicts that traits under divergent selection and those that play a role in premating isolation should be tightly linked in order to facilitate speciation [65,86].…”

“…By contrast, while it is widely acknowledged that chemical signals play a role in animal premating isolation [68,69], their role as drivers of sympatric speciation is much less studied. Lepidoptera is the order that has the most information on volatiles involved in sexual recognition: more than 2000 sex pheromones have been identified in moths, and an additional eight have been identified in day flying butterflies [70][71][72]. The function of sex chemicals in promoting species recognition and ensuring reproductive isolation in moths has been extensively demonstrated [72], while in butterflies, experimental evidence of such phenomena is less abundant [10,71,73,74].…”

“…Lepidoptera is the order that has the most information on volatiles involved in sexual recognition: more than 2000 sex pheromones have been identified in moths, and an additional eight have been identified in day flying butterflies [70][71][72]. The function of sex chemicals in promoting species recognition and ensuring reproductive isolation in moths has been extensively demonstrated [72], while in butterflies, experimental evidence of such phenomena is less abundant [10,71,73,74]. This is probably because researchers usually assume that butterflies should mainly rely on mating systems based on visual signals suited to their diurnal habits.…”

“…Also, our results suggest that both male chemical production and female preference in Heliconius are heritable traits with a simple genetic basis. In fact, recent studies have pinpointed candidate regions implicated in the production of male pheromone components in Heliconius [71]. However, to date, the genetic basis controlling female assortative mating behaviours remains largely unknown (but see [88]).…”

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

“…Behavioral experiments reveal that chemical signaling in Heliconius erato, H. melpomene , and H. timareta is important for female mate choice (Darragh et al, 2017; Mérot, Frérot, Leppik, & Joron, 2015). Previous studies have shown that Heliconius cydno and H. melpomene respond to both con‐ and heterospecific androconial chemical bouquets (Byers et al, 2019), and have identified an individual compound that is electrophysiologically and behaviorally active. Furthermore, studies of H. cydno , H. doris , H. hecale , H. ismenius , H. melpomene , H. pardalinus , H. sara , and H. timareta from Panama, Colombia, Ecuador, and Peru found that major compounds differ between species (Mann et al, 2017; Mérot et al, 2015), suggesting a potential role in reproductive isolation.…”