Abstract
BackgroundFemale sex pheromones attracting mating partners over long distances are a major determinant of reproductive isolation and speciation in Lepidoptera. Males can also produce sex pheromones but their study, particularly in butterflies, has received little attention. A detailed comparison of sex pheromones in male butterflies with those of female moths would reveal patterns of conservation versus novelty in the associated behaviours, biosynthetic pathways, compounds, scent-releasing structures and receiving systems. Here we assess whether the African butterfly Bicyclus anynana, for which genetic, genomic, phylogenetic, ecological and ethological tools are available, represents a relevant model to contribute to such comparative studies.Methodology/Principal FindingsUsing a multidisciplinary approach, we determined the chemical composition of the male sex pheromone (MSP) in the African butterfly B. anynana, and demonstrated its behavioural activity. First, we identified three compounds forming the presumptive MSP, namely (Z)-9-tetradecenol (Z9-14:OH), hexadecanal (16:Ald ) and 6,10,14-trimethylpentadecan-2-ol (6,10,14-trime-15-2-ol), and produced by the male secondary sexual structures, the androconia. Second, we described the male courtship sequence and found that males with artificially reduced amounts of MSP have a reduced mating success in semi-field conditions. Finally, we could restore the mating success of these males by perfuming them with the synthetic MSP.Conclusions/SignificanceThis study provides one of the first integrative analyses of a MSP in butterflies. The toolkit it has developed will enable the investigation of the type of information about male quality that is conveyed by the MSP in intraspecific communication. Interestingly, the chemical structure of B. anynana MSP is similar to some sex pheromones of female moths making a direct comparison of pheromone biosynthesis between male butterflies and female moths relevant to future research. Such a comparison will in turn contribute to understanding the evolution of sex pheromone production and reception in butterflies.
Highlights
Studies on sexual communication are biased towards visually-based traits, chemical communication using sex pheromones is predominant from arthropods to mammals for ensuring mate choice and reproduction (e.g. [1,2,3,4])
A detailed comparative analysis of the biosynthesis, chemical structure, use and function of sex pheromones between male butterflies and female moths could reveal the extent of conservation versus evolutionary novelties for the behaviours, biosynthetic pathways, compounds, scent-structures and receiving systems involved in communication through sex pheromones
We have identified three components included in the sex pheromone of B. anynana males, namely Z9-14:OH, 16:Ald and 6,10,14-trime-15-2-ol
Summary
Studies on sexual communication are biased towards visually-based traits, chemical communication using sex pheromones is predominant from arthropods to mammals for ensuring mate choice and reproduction (e.g. [1,2,3,4]). Male olfactory displays in Lepidoptera are thought to be involved in mate assessment as they can convey information about the prospective mates [39,40], such as quality and quantity of nuptial gifts [21], or male size [25] (but see [41]) The diversity of both the chemical compounds and the scent-structures associated with male pheromones [7,37] could reflect differences across the sexes in terms of patterns of recruitment of pathways at the genetical and developmental levels [42]. A detailed comparison of sex pheromones in male butterflies with those of female moths would reveal patterns of conservation versus novelty in the associated behaviours, biosynthetic pathways, compounds, scent-releasing structures and receiving systems. We assess whether the African butterfly Bicyclus anynana, for which genetic, genomic, phylogenetic, ecological and ethological tools are available, represents a relevant model to contribute to such comparative studies
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