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The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis.

Nieberding, CM ; de Vos, H ; Schneider, MV ; Lassance, Jean-Marc LU ; Estramil, N ; Andersson, J ; Bång, J ; Hedenström, E ; Löfstedt, Christer LU and Brakefield, PM (2008) In PLoS ONE 3(e2751). p.1-12
Abstract
BACKGROUND: Female 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... (More)
BACKGROUND: Female 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 FINDINGS: Using 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/SIGNIFICANCE: This 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 (Less)
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author
; ; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
PLoS ONE
volume
3
issue
e2751
pages
1 - 12
publisher
Public Library of Science (PLoS)
external identifiers
  • wos:000264302900022
  • scopus:50249165893
  • pmid:18648495
ISSN
1932-6203
DOI
10.1371/journal.pone.0002751
project
Evolutionary mechanisms of pheromone divergence in Lepidoptera
language
English
LU publication?
yes
id
ac1986ed-2809-48b8-9a59-1f1833bd6eba (old id 1428588)
date added to LUP
2016-04-01 12:58:14
date last changed
2024-05-09 01:00:38
@article{ac1986ed-2809-48b8-9a59-1f1833bd6eba,
  abstract     = {{BACKGROUND: Female 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 FINDINGS: Using 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/SIGNIFICANCE: This 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}},
  author       = {{Nieberding, CM and de Vos, H and Schneider, MV and Lassance, Jean-Marc and Estramil, N and Andersson, J and Bång, J and Hedenström, E and Löfstedt, Christer and Brakefield, PM}},
  issn         = {{1932-6203}},
  language     = {{eng}},
  number       = {{e2751}},
  pages        = {{1--12}},
  publisher    = {{Public Library of Science (PLoS)}},
  series       = {{PLoS ONE}},
  title        = {{The male sex pheromone of the butterfly <i>Bicyclus anynana</i>: towards an evolutionary analysis.}},
  url          = {{http://dx.doi.org/10.1371/journal.pone.0002751}},
  doi          = {{10.1371/journal.pone.0002751}},
  volume       = {{3}},
  year         = {{2008}},
}