Sexual Selection Drives the Evolution of Antiaphrodisiac Pheromones in Butterflies

Abstract

Competition for mates has resulted in sophisticated mechanisms of male control over female reproduction. Antiaphrodisiacs are pheromones transferred from males to females during mating that reduce attractiveness of females to subsequent courting males.Antiaphrodisiacs generally help unreceptive females reduce male harassment. However, lack of control over pheromone release by females and male control over the amount transferred provides males an opportunity to use antiaphrodisiacs to delay remating by females that have returned to a receptive state. We propose a model for the evolution of antiaphrodisiacs under the influence of intrasexual selection, and determine whether changes in this signal in 11 species of Heliconius butterflies are consistent with two predictions of the model. First, we find that as predicted, male-contributed chemical mixtures are complex and highly variable across species, with limited phylogenetic signal. Second, differences in rates of evolution in pheromone composition between two major clades of Heliconius are as expected: the clade with a greater potential for male-male competition (polyandrous) shows a faster rate of divergence than the one with typically monoandrous mating system. Taken together, our results provide evidence that for females, antiaphrodisiacs can be both honest signals of receptivity (helping reduce harassment) and chastity belts (a male-imposed reduction in remating). K E Y W O R D S :Female mating receptivity, Heliconius, male-male competition, male control on female reproduction, sexual conflict, signal evolution.Male control over female mating frequency is common in nature and involves remarkable morphological, behavioral, and physiological adaptations aimed at manipulating female receptivity or discouraging advances by other males (e.g., Parker 1970, Simmons 2001. Common mechanisms include the transfer of seminal fluid proteins, donation of nuptial gifts, formation of mating plugs, and mate guarding (Thornhill and Alcock 1983;Simmons 2001). The evolution of such strategies is the result of selection on males to reduce sperm competition when females mate repeatedly within a breeding period. Females often obtain direct

Sex pheromone biosynthetic pathways are conserved between moths and the butterfly Bicyclus anynana

“…We show that FA desaturases and reductases orthologous to moth-biosynthetic genes are active in a butterfly, specifically B. anynana ; yet, male abdominal glands of several Heliconius butterflies have also been shown to contain a large variety of FA-derived compounds including saturated and unsaturated long-chain alcohol and acetate chemicals4958. This suggests that these pathways and enzymes are likely conserved in other butterfly systems.…”

“…This suggests that these pathways and enzymes are likely conserved in other butterfly systems. Although no detailed studies have investigated as yet the molecular underpinnings of these secretions, it is realistic to suggest that at least some of the predicted orthologous FAD and FAR genes have remained functional, however different the ethological role that FA derivatives might fulfil in butterflies in general49. Altogether, this supports the idea that moth-like biochemical pathways and the underlying genetic networks have survived over long evolutionary times across butterfly lineages to act in the de novo biosynthesis of diverse butterfly chemical secretions.…”

“…In addition, we explore other butterfly genomes and provide evidence for the conservation of biosynthetic gene clades in important butterfly systems such as Danaus and Heliconius . Altogether, our findings bring the first critical evidence to reconcile the evolutionary history of genes that are involved in the production of volatile chemicals in Bicyclus , with appropriate tools to start investigating the molecular underpinnings of FA secretions49, utilized within the butterflies.…”

Selection on male sex pheromone composition contributes to butterfly reproductive isolation

“…Yet, the behaviour of B. anynana does not suggest the existence of anti-aphrodisiacs (e.g. no pupal mating like in Heliconius [51]). Anti-aphrodisiacs are transferred between male and female abdomens, which were not analysed here.…”

An insect anti-antiaphrodisiac

“…Such variability in the starting amount can result in a female being ready to mate well before a large load of antiaphrodisiac is sufficiently depleted for her to be attractive again, or being prematurely courted if the male transfers too little. Such signaling uncertainty is potentially costly to the fitness of both females and males, and should create selective pressure to produce a more accurate signaling system that incorporates information beyond the amount of remaining antiaphrodisiac (Estrada et al, 2011). To date, the only mechanism shown to allow females to counteract the effect of an antiaphrodisiac is in Drosophila , in which females actively eject mating-transferred cis-vaccenyl acetate from their reproductive tract (Laturney and Billeter, 2016).…”