User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Common Practice Solvent Extraction Does not Reflect Actual Emission of a Sex Pheromone During Butterfly Courtship

Primary tabs

download
  • Open access
  • PDF
  • 1.21 M
Visser, Bertanne [UCL] Dublon, Ian A. N. [UCL] Heuskin, Stéphanie [UCL] Laval, Florent [Analytical Chemistry, AgroBioChem Department, Gembloux Agro-Bio Tech, Université de Liège, Gembloux, Belgium] Bacquet, Paul M. B. [UCL] Nieberding, Caroline M. [UCL]

Olfactory communication can be of critical importance for mate choice decisions. Lepidoptera are key model systems for understanding olfactory communication, particularly considering sex pheromone signaling in the context of sexual selection. Solvent extraction or rinsing of pheromone-producing structures is a widespread method for quantifying sex pheromones, but such measures reflect what is stored and may not represent what is actually emitted by an individual during courtship. Here, we address this point for the first time by quantifying the components of the male sex pheromone (MSP) of interacting Bicyclus anynana butterflies, a species for which much information is available onthe role played by MSPs in affecting mating success. Using headspace sampling during courtship and solvent extraction after completion of experiments using the same males, we were able to track individual traits. Our results show that solvent extracts do not reflect quantities of MSP components emitted by live butterflies. We further show that MSP amounts obtained using headspace sampling correlated with male mating success, but solvent extracts did not. Our results further strongly suggest that males actively control MSP emission when faced with increased male-male competition. Common practice solvent extracts may thus not serve as an adequate proxy for male sex pheromone signaling as they are perceived by choosy females. Our study serves as a proof of principle that quantification of male sex pheromone components depends on the method of collection, which could apply to many other insects using short-range chemical signals. This affects our understanding of how sexual selection shapes the evolution of sexually-selected chemical traits.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2018
Language Anglais
Journal information "Frontiers in Ecology and Evolution" - Vol. 6, no.154, p. 1-10 (2018)
Peer reviewed yes
Publisher Frontiers Research Foundation
issn 2296-701X
e-issn 2296-701X
Publication status Publié
Affiliation UCL - SST/ELI/ELIB - Biodiversity
Links
  1. Andersson J., Borg-Karlson A.-K., Vongvanich N., Wiklund C., Male sex pheromone release and female mate choice in a butterfly, 10.1242/jeb.02726
  2. Bacquet P. M. B., Brattstrom O., Wang H.- L., Allen C. E., Lofstedt C., Brakefield P. M., Nieberding C. M., Selection on male sex pheromone composition contributes to butterfly reproductive isolation, 10.1098/rspb.2014.2734
  3. Birch M C, Poppy G M, Baker T C, Scents and Eversible Scent Structures of Male Moths, 10.1146/annurev.en.35.010190.000325
  4. Boughman Janette Wenrick, Divergent sexual selection enhances reproductive isolation in sticklebacks, 10.1038/35082064
  5. Brakefield P. M., Beldade P., Zwaan B. J., The African Butterfly Bicyclus anynana: A Model for Evolutionary Genetics and Evolutionary Developmental Biology, 10.1101/pdb.emo122
  6. Byrne Kevin J., Gore William E., Pearce Glenn T., Silverstein Robert M., Porapak-Q collection of airborne organic compounds serving as models for insect pheromones, 10.1007/bf00987716
  7. Clearwater John R., Chemistry and function of a pheromone produced by the male of the southern armyworm Pseudaletia separata, 10.1016/0022-1910(72)90202-8
  8. Costanzo Katie, Monteiro Antónia, The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana, 10.1098/rspb.2006.3729
  9. Cross John H., Byler Russell C., Cassidy Robert F., Silverstein Robert M., Greenblatt Richard E., Burkholder Wendell E., Levinson A. R., Levinson H. Z., Porapak-Q collection of pheromone components and isolation of (Z)- and (E)-14-methyl-8-hexadecenal, sex pheromone components, from the females of four species ofTrogoderma (Coleoptera: Dermestidae), 10.1007/bf00988811
  10. Darragh Kathy, Vanjari Sohini, Mann Florian, Gonzalez-Rojas Maria F., Morrison Colin R., Salazar Camilo, Pardo-Diaz Carolina, Merrill Richard M., McMillan W. Owen, Schulz Stefan, Jiggins Chris D., Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice, 10.7717/peerj.3953
  11. Darwin, On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life (1859)
  12. Dion Emilie, Monteiro Antónia, Yew Joanne Y., Phenotypic plasticity in sex pheromone production in Bicyclus anynana butterflies, 10.1038/srep39002
  13. Dion Emilie, Pui Li Xian, Monteiro Antonia, Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring, 10.1101/214635
  14. Foster Stephen P., Anderson Karin G., Casas Jérôme, The Dynamics of Pheromone Gland Synthesis and Release: a Paradigm Shift for Understanding Sex Pheromone Quantity in Female Moths, 10.1007/s10886-018-0963-z
  15. Greenfield Michael D., Moth Sex Pheromones: An Evolutionary Perspective, 10.2307/3494597
  16. Groot Astrid T., Dekker Teun, Heckel David G., The Genetic Basis of Pheromone Evolution in Moths, 10.1146/annurev-ento-010715-023638
  17. Groot A. T., Horovitz J. L., Hamilton J., Santangelo R. G., Schal C., Gould F., Experimental evidence for interspecific directional selection on moth pheromone communication, 10.1073/pnas.0508609103
  18. Heuskin Stéphanie, Vanderplanck Maryse, Bacquet Paul, Holveck Marie-Jeanne, Kaltenpoth Martin, Engl Tobias, Pels Christophe, Taverne Cédric, Lognay Georges, Nieberding Caroline M., The composition of cuticular compounds indicates body parts, sex and age in the model butterfly Bicyclus anynana (Lepidoptera), 10.3389/fevo.2014.00037
  19. Hill A. S., Card� R. T., Kido H., Roelofs W. L., Sex pheromone of the orange tortrix moth,Argyrotaenia citrana (Lepidoptera: Tortricidae), 10.1007/bf00987870
  20. HIRAI Kazuo, Male Scent Emitted by Armyworms, Pseudaletia unipuncta and P. separata (Lepidoptera : Noctuidae), 10.1303/aez.15.310
  21. Holveck Marie-Jeanne, Gauthier Anne-Laure, Nieberding Caroline M., Dense, small and male-biased cages exacerbate male–male competition and reduce female choosiness in Bicyclus anynana, 10.1016/j.anbehav.2015.03.025
  22. Johansson Björn G., Jones Therésa M., The role of chemical communication in mate choice, 10.1111/j.1469-185x.2007.00009.x
  23. Joron Mathieu, Brakefield Paul M., Captivity masks inbreeding effects on male mating success in butterflies, 10.1038/nature01713
  24. KARLSON P., LÜSCHER M., ‘Pheromones’: a New Term for a Class of Biologically Active Substances, 10.1038/183055a0
  25. KUWAHARA Yasumasa, Scent Scale Substances of Male Pieris melete MENETRIES (Pieridae : Lepidoptera), 10.1303/aez.14.350
  26. Miller Christine W., Svensson Erik I., Sexual Selection in Complex Environments, 10.1146/annurev-ento-011613-162044
  27. Nieberding Caroline M., de Vos Helene, Schneider Maria V., Lassance Jean-Marc, Estramil Natalia, Andersson Jimmy, Bång Joakim, Hedenström Erik, Löfstedt Christer, Brakefield Paul M., The Male Sex Pheromone of the Butterfly Bicyclus anynana: Towards an Evolutionary Analysis, 10.1371/journal.pone.0002751
  28. Nieberding Caroline M., Fischer Klaus, Saastamoinen Marjo, Allen Cerisse E., Wallin Erika A., Hedenström Erik, Brakefield Paul M., Cracking the olfactory code of a butterfly: the scent of ageing : The scent of ageing in a butterfly, 10.1111/j.1461-0248.2012.01748.x
  29. Nieberding Caroline M., Holveck Marie-Jeanne, Laboratory social environment biases mating outcome: a first quantitative synthesis in a butterfly, 10.1007/s00265-017-2346-9
  30. Nieberding Caroline Marie, Holveck Marie-Jeanne, Commentary on Kehl et al. “Young male mating success is associated with sperm number but not with male sex pheromone titres” : Unnatural experimental conditions inflate the importance of male courtship activity on mating success in a butterfly, 10.1186/s12983-018-0256-y
  31. Nieberding Caroline M., San Martin Gilles, Saenko Suzanne, Allen Cerisse E., Brakefield Paul M., Visser Bertanne, Sexual selection contributes to partial restoration of phenotypic robustness in a butterfly, 10.1038/s41598-018-32132-8
  32. Panhuis Tami M., Butlin Roger, Zuk Marlene, Tregenza Tom, Sexual selection and speciation, 10.1016/s0169-5347(01)02160-7
  33. Percy Miss J. E., Gardiner Miss E. J., Weatherston J., STUDIES OF PHYSIOLOGICALLY ACTIVE ARTHROPOD SECRETIONS: VI. EVIDENCE FOR A SEX PHEROMONE IN FEMALE ORGYIA LEUCOSTIGMA (LEPIDOPTERA: LYMANTRIDAE), 10.4039/ent103706-5
  34. PHELAN P. L., BAKER T. C., Evolution of Male Pheromones in Moths: Reproductive Isolation Through Sexual Selection?, 10.1126/science.235.4785.205
  35. Prudic K. L., Jeon C., Cao H., Monteiro A., Developmental Plasticity in Sexual Roles of Butterfly Species Drives Mutual Sexual Ornamentation, 10.1126/science.1197114
  36. R: A Language and Environment for Statistical Computing2016
  37. Rodríguez Rafael L., Boughman Janette W., Gray David A., Hebets Eileen A., Höbel Gerlinde, Symes Laurel B., Diversification under sexual selection: the relative roles of mate preference strength and the degree of divergence in mate preferences, 10.1111/ele.12142
  38. Roelofs W., Hill A., Card� R., Sex pheromone components of the redbanded leafroller,Argyrotaenia velutinana (Lepidoptera: Tortricidae), 10.1007/bf00987721
  39. Mate choice and sexual selection in a model butterfly species, Bicyclus anynana: state of the art922 San MartinG. BacquetP. NieberdingC. M. Proc. Neth. Entomol. Soc.222011
  40. Sanders C. J., Weatherston J., SEX PHEROMONE OF THE EASTERN SPRUCE BUDWORM (LEPIDOPTERA: TORTRICIDAE): OPTIMUM BLEND OF TRANS- AND CIS-11-TETRADECENAL, 10.4039/ent1081285-11
  41. Sappington Thomas W., Taylor Orley R., Genetic sources of pheromone variation inColias eurytheme butterflies, 10.1007/bf00988084
  42. Smadja C, Butlin R K, On the scent of speciation: the chemosensory system and its role in premating isolation, 10.1038/hdy.2008.55
  43. Tóth Miklós, Buser Hans-Rudolf, Simple method for collecting volatile compounds from single insects and other point sources for gas chromatographic analysis, 10.1016/0021-9673(92)85060-7
  44. Umbers Kate D. L., Symonds Matthew R. E., Kokko Hanna, The Mothematics of Female Pheromone Signaling: Strategies for Aging Virgins, 10.1086/679614
  45. van Bergen E., Brakefield P. M., Heuskin S., Zwaan B. J., Nieberding C. M., The scent of inbreeding: a male sex pheromone betrays inbred males, 10.1098/rspb.2013.0102
  46. Visser Bertanne, Dublon Ian A. N., Heuskin Stephanie, Laval Forent, Bacquet Paul M. B., Lognay Georges, Nieberding Caroline M., Common practice solvent extraction does not reflect actual emission of a sex pheromone during butterfly courtship, 10.1101/270462
  47. WallaceA. R. SmithC. H. Note on Sexual Selection (S459: 1892)1892
  48. Westerman Erica L., Chirathivat Napon, Schyling Elizabeth, Monteiro Antónia, MATE PREFERENCE FOR A PHENOTYPICALLY PLASTIC TRAIT IS LEARNED, AND MAY FACILITATE PREFERENCE-PHENOTYPE MATCHING : SEXUALLY DIMORPHIC MATE CHOICE PLASTICITY, 10.1111/evo.12381
  49. Westerman E. L., Hodgins-Davis A., Dinwiddie A., Monteiro A., Biased learning affects mate choice in a butterfly, 10.1073/pnas.1118378109
  50. Wyatt, Pheromones and Animal Behaviour: Chemical Signals and Signatures (2014)
Bibliographic reference Visser, Bertanne ; Dublon, Ian A. N. ; Heuskin, Stéphanie ; Laval, Florent ; Bacquet, Paul M. B. ; et. al. Common Practice Solvent Extraction Does not Reflect Actual Emission of a Sex Pheromone During Butterfly Courtship. In: Frontiers in Ecology and Evolution, Vol. 6, no.154, p. 1-10 (2018)
Permanent URL http://hdl.handle.net/2078.1/216622