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The scent of inbreeding: a male sex pheromone betrays inbred males

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van Bergen, Erik [Institute of Biology Leiden, The Netherlands] Brakefield, Paul M. [Institute of Biology Leiden, The Netherlands] Bas , J. Zwaan [Institute of Biology Leiden, The Netherlands] Heuskin, Stéphanie [UCL] Nieberding, Caroline M. [UCL]

Inbreeding depression results from mating among genetically related individuals and impairs reproductive success. The decrease in male mating success is usually attributed to an impact on multiple fitness-related traits that reduce the general condition of inbred males. Here, we find that the production of the male sex pheromone is reduced significantly by inbreeding in the butterfly Bicyclus anynana. Other traits indicative of the general condition, including flight performance, are also negatively affected in male butterflies by inbreeding. Yet, we unambiguously show that only the pro- duction of male pheromones affects mating success. Thus, this pheromone signal informs females about the inbreeding status of their mating partners. We also identify the specific chemical component (hexadecanal) probably responsible for the decrease in male mating success. Our results advocate giving increased attention to olfactory communication as a major causal factor of mate-choice decisions and sexual selection.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2013
Language Anglais
Journal information "Proceedings of the Royal Society of London. Series B, Biological Sciences" - Vol. 280, p. 1-8 (2013)
Peer reviewed yes
issn 0080-4649
Publication status Publié
Affiliation UCL - SST/ELI/ELIB - Biodiversity
Keywords inbreeding depression ; male sex pheromone ; mating success ; flight performance ; female choice ; 3123
Links
  1. Charlesworth Deborah, Willis John H., The genetics of inbreeding depression, 10.1038/nrg2664
  2. Miller P. S., Glasner J., Hedrick P. W., Inbreeding depression and male-mating behavior inDrosophila melanogaster, 10.1007/bf02424449
  3. Joron Mathieu, Brakefield Paul M., Captivity masks inbreeding effects on male mating success in butterflies, 10.1038/nature01713
  4. Mariette Mylene, Kelley Jennifer L, Brooks Robert, Evans Jonathan P, The Effects of Inbreeding on Male Courtship Behaviour and Coloration in Guppies, 10.1111/j.1439-0310.2006.01236.x
  5. Meagher S., Male-male competition magnifies inbreeding depression in wild house mice, 10.1073/pnas.060284797
  6. Keller L, Inbreeding effects in wild populations, 10.1016/s0169-5347(02)02489-8
  7. Bolund Elisabeth, Martin Katrin, Kempenaers Bart, Forstmeier Wolfgang, Inbreeding depression of sexually selected traits and attractiveness in the zebra finch, 10.1016/j.anbehav.2010.01.014
  8. Thornhill Randy, Sexual Selection and Paternal Investment in Insects, 10.1086/283055
  9. Côte I.M., Hunte W., Male and female mate choice in the redlip blenny: why bigger is better, 10.1016/s0003-3472(89)80067-3
  10. BOGGS C. L., GILBERT L. E., Male Contribution to Egg Production in Butterflies: Evidence for Transfer of Nutrients at Mating, 10.1126/science.206.4414.83
  11. Saccheri Ilik J., Brakefield Paul M., Nichols Richard A., Severe Inbreeding Depression and Rapid Fitness Rebound in the Butterfly Bicyclus anynana (Satyridae), 10.2307/2410758
  12. Saccheri I. J., Lloyd H. D., Helyar S. J., Brakefield P. M., Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly, 10.1098/rspb.2004.2903
  13. Aspi Jouni, Inbreeding and outbreeding depression in male courtship song characters in Drosophila montana, 10.1046/j.1365-2540.2000.00655.x
  14. Van Oosterhout C., Trigg R. E., Carvalho G. R., Magurran A. E., Hauser L., Shaw P. W., Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots : Inbreeding depression of sexual traits, 10.1046/j.1420-9101.2003.00511.x
  15. Reid J., Arcese P., Cassidy AliceL.E.V, Marr A., Smith JamesN.M, Keller L., Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia), 10.1098/rspb.2004.2983
  16. Drayton, Evolution, 64, 3069 (2010)
  17. Bentsen Caroline L., Hunt John, Jennions Michael D., Brooks Robert, Complex Multivariate Sexual Selection on Male Acoustic Signaling in a Wild Population ofTeleogryllus commodus, 10.1086/501376
  18. Iyengar Vikram K., Rossini Carmen, Eisner Thomas, Precopulatory assessment of male quality in an arctiid moth (Utetheisa ornatrix): hydroxydanaidal is the only criterion of choice, 10.1007/s002650000292
  19. Rantala M. J., Jokinen I., Kortet R., Vainikka A., Suhonen J., Do pheromones reveal male immunocompetence?, 10.1098/rspb.2002.2056
  20. Lopez P., Martin J., Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response, 10.1098/rsbl.2005.0360
  21. Ruther J., Matschke M., Garbe L.-A., Steiner S., Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis, 10.1098/rspb.2009.0738
  22. Ilmonen Petteri, Stundner Gloria, ThoSZ Michaela, Penn Dustin J., Females prefer the scent of outbred males: good-genes-as-heterozygosity?, 10.1186/1471-2148-9-104
  23. Thom Michael D., Stockley Paula, Jury Francine, Ollier William E.R., Beynon Robert J., Hurst Jane L., The Direct Assessment of Genetic Heterozygosity through Scent in the Mouse, 10.1016/j.cub.2008.03.056
  24. THOß M., ILMONEN P., MUSOLF K., PENN D. J., Major histocompatibility complex heterozygosity enhances reproductive success : HETEROZYGOSITY ENHANCES REPRODUCTIVE SUCCESS, 10.1111/j.1365-294x.2011.05009.x
  25. Polkki M., Krams I., Kangassalo K., Rantala M. J., Inbreeding affects sexual signalling in males but not females of Tenebrio molitor, 10.1098/rsbl.2011.1135
  26. Wyatt Tristram D., Fifty years of pheromones, 10.1038/457262a
  27. Oosterhout Cock van, Zijlstra Wilte G., van Heuven Marianne K., Brakefield Paul M., INBREEDING DEPRESSION AND GENETIC LOAD IN LABORATORY METAPOPULATIONS OF THE BUTTERFLY BICYCLUS ANYNANA, 10.1554/0014-3820(2000)054[0218:idagli]2.0.co;2
  28. BRAKEFIELD PAUL M., REITSMA NICO, Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi, 10.1111/j.1365-2311.1991.tb00220.x
  29. WINDIG JACK J., BRAKEFIELD PAUL M., REITSMA NICO, WILSON JOHN G. M., Seasonal polyphenism in the wild: survey of wing patterns in five species of Bicyclus butterflies in Malawi, 10.1111/j.1365-2311.1994.tb00420.x
  30. Costanzo K., Monteiro A., The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana, 10.1098/rspb.2006.3729
  31. 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
  32. 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
  33. Brakefield P. M., El Filali E., Van Der Laan R., Breuker C. J., Saccheri I. J., Zwaan B., Effective population size, reproductive success and sperm precedence in the butterfly, Bicyclus anynana, in captivity : Mating success in a captive butterfly population, 10.1046/j.1420-9101.2001.00248.x
  34. VAN'T HOF A. E., ZWAAN B. J., SACCHERI I. J., DALY D., BOT A. N. M., BRAKEFIELD P. M., Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana, 10.1111/j.1471-8286.2004.00870.x
  35. Heuskin Stéphanie, Godin Bruno, Leroy Pascal, Capella Quentin, Wathelet Jean-Paul, Verheggen François, Haubruge Eric, Lognay Georges, Fast gas chromatography characterisation of purified semiochemicals from essential oils of Matricaria chamomilla L. (Asteraceae) and Nepeta cataria L. (Lamiaceae), 10.1016/j.chroma.2008.09.109
  36. Saastamoinen Marjo, van der Sterren Dominique, Vastenhout Nienke, Zwaan Bas J., Brakefield Paul M., Predictive Adaptive Responses: Condition‐Dependent Impact of Adult Nutrition and Flight in the Tropical ButterflyBicyclus anynana, 10.1086/657038
  37. DeRose Marc A., Roff Derek A., A Comparison of Inbreeding Depression in Life-History and Morphological Traits in Animals, 10.2307/2640831
  38. Roff Derek A., Emerson Kevin, EPISTASIS AND DOMINANCE: EVIDENCE FOR DIFFERENTIAL EFFECTS IN LIFE-HISTORY VERSUS MORPHOLOGICAL TRAITS, 10.1111/j.0014-3820.2006.tb01836.x
  39. Kempenaers Bart, Mate Choice and Genetic Quality: A Review of the Heterozygosity Theory, Advances in the Study of Behavior (2007) ISBN:9780120045372 p.189-278, 10.1016/s0065-3454(07)37005-8
  40. Whitlock Michael C., Agrawal Aneil F., PURGING THE GENOME WITH SEXUAL SELECTION: REDUCING MUTATION LOAD THROUGH SELECTION ON MALES, 10.1111/j.1558-5646.2008.00558.x
  41. Roldan E. R. S., Cassinello J., Abaigar T., Gomendio M., Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate, 10.1098/rspb.1998.0288
  42. Gage Matthew J.G., Surridge Alison K., Tomkins Joseph L., Green Emma, Wiskin Louise, Bell Diana J., Hewitt Godfrey M., Reduced Heterozygosity Depresses Sperm Quality in Wild Rabbits, Oryctolagus cuniculus, 10.1016/j.cub.2006.02.059
  43. Berwaerts K., Van Dyck H., Aerts P., Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria, 10.1046/j.1365-2435.2002.00650.x
  44. Oostra V., de Jong M. A., Invergo B. M., Kesbeke F., Wende F., Brakefield P. M., Zwaan B. J., Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly, 10.1098/rspb.2010.1560
  45. Amrein Hubert, Thorne Natasha, Gustatory Perception and Behavior in Drosophila melanogaster, 10.1016/j.cub.2005.08.021
  46. Ebbs Michelle L., Amrein Hubert, Taste and pheromone perception in the fruit fly Drosophila melanogaster, 10.1007/s00424-007-0246-y
  47. Miyamoto Tetsuya, Amrein Hubert, Suppression of male courtship by a Drosophila pheromone receptor, 10.1038/nn.2161
  48. CANDOLIN ULRIKA, The use of multiple cues in mate choice, 10.1017/s1464793103006158
  49. Bretman Amanda, Westmancoat James D., Gage Matthew J.G., Chapman Tracey, Males Use Multiple, Redundant Cues to Detect Mating Rivals, 10.1016/j.cub.2011.03.008
  50. Coleman Seth W., Taxonomic and sensory biases in the mate-choice literature: there are far too few studies of chemical and multimodal communication, 10.1007/s10211-008-0050-5
  51. Campbell-Palmer Róisín, Rosell Frank, The importance of chemical communication studies to mammalian conservation biology: A review, 10.1016/j.biocon.2011.04.028
Bibliographic reference van Bergen, Erik ; Brakefield, Paul M. ; Bas , J. Zwaan ; Heuskin, Stéphanie ; Nieberding, Caroline M.. The scent of inbreeding: a male sex pheromone betrays inbred males. In: Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 280, p. 1-8 (2013)
Permanent URL http://hdl.handle.net/2078.1/125723