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

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1758, 2013, Pages

  van Bergen, Erik ^a,b   Brakefield, Paul M ^a,b   Heuskin, Stéphanie ^c   Zwaan, Bas J ^a,d   Nieberding, Caroline M ^e  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY MUSEUM OF ZOOLOGY   (United Kingdom)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e Académie Louvain   (Belgium)

Author keywords

Female choice; Flight performance; Inbreeding depression; Male sex pheromone; Mating success

Indexed keywords

BUTTERFLY; DECISION ANALYSIS; FITNESS; GENETICALLY MODIFIED ORGANISM; INBREEDING; LIFE HISTORY TRAIT; MATE CHOICE; MATING BEHAVIOR; OLFACTORY CUE; REPRODUCTIVE SUCCESS; SEX PHEROMONE;

EID: 84874776911     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.0102     Document Type: Article

References (56)

1. Charlesworth D, Willis JH. 2009 The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783-796. (doi:10.1038/nrg2664)
2. Miller PS, Glasner J, Hedrick PW. 1993 Inbreeding depression and male-mating behavior in Drosophila melanogaster. Genetica 88, 29-36. (doi:10.1007/bf02424449)
3. Joron M, Brakefield PM. 2003 Captivity masks inbreeding effects on male mating success in butterflies. Nature 424, 191-194. (doi:10.1038/nature01713)
4. Mariette M, Kelley JL, Brooks R, Evans JP. 2006 The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112, 807-814. (doi:10.1111/j.1439-0310.2006.01236.x)
5. Meagher S, Penn DJ, Potts WK. 2000 Male-male competition magnifies inbreeding depression in wild house mice. Proc. Natl Acad. Sci. USA 97, 3324-3329. (doi:10.1073/pnas. 060284797)
6. Keller LF, Waller DM. 2002 Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230-241. (doi:10.1016/s0169-5347(02)02489-8)
7. Bolund E, Martin K, Kempenaers B, Forstmeier W. 2010 Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Anim. Behav. 79, 947-955. (doi:10.1016/j.anbehav. 2010.01.014)
8. Thornhill R. 1976 Sexual selection and paternal investment in insects. Am. Nat. 110, 153-163. (doi:10.1086/283055)
9. Cote IM, Hunte W. 1989 Male and female mate choice in the redlip blenny: why bigger is better. Anim. Behav. 38, 78-88. (doi:10.1016/s0003-3472(89)80067-3)
10. Boggs CL, Gilbert LE. 1979 Male contribution to egg-production in butterflies: evidence for transfer of nutrients at mating. Science 206, 83-84. (doi:10.1126/science.206.4414.83)
11. Saccheri IJ, Brakefield PM, Nichols RA. 1996 Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50, 2000-2013. (doi:10.2307/2410758)
12. Saccheri IJ, Lloyd HD, Helyar SJ, Brakefield PM. 2005 Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly. Proc. R. Soc. B 272, 39-46. (doi:10.1098/rspb.2004.2903)
13. Aspi J. 2000 Inbreeding and outbreeding depression in male courtship song characters in Drosophila montana. Heredity 84, 273-282. (doi:10.1046/j. 1365-2540.2000.00655.x)
14. van Oosterhout C, Trigg RE, Carvalho GR, Magurran AE, Hauser L, Shaw PW. 2003 Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J. Evol. Biol. 16, 273-281. (doi:10.1046/j.1420-9101.2003.00511.x)
15. Reid JM, Arcese P, Cassidy A, Marr AB, Smith JNM, Keller LF. 2005 Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia). Proc. R. Soc. B 272, 481-487. (doi:10.1098/rspb.2004.2983)
16. Drayton JM, Milner RNC, Hunt J, Jennions MD. 2010 Inbreeding and advertisement calling in the cricket Teleogryllus commodus: laboratory and field experiments. Evolution 64, 3069-3083. (doi:10. 1111/j.1558-5646.2010.01053.x)
17. Bentsen CL, Hunt J, Jennions MD, Brooks R. 2006 Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus. Am. Nat. 167, E102-E116. (doi:10.1086/501376)
18. Iyengar VK, Rossini C, Eisner T. 2001 Precopulatory assessment of male quality in an arctiid moth (Utetheisa ornatrix): hydroxydanaidal is the only criterion of choice. Behav. Ecol. Sociobiol. 49, 283-288. (doi:10.1007/s002650000292)
19. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J. 2002 Do pheromones reveal male immunocompetence? Proc. R. Soc. Lond. B 269, 1681-1685. (doi:10.1098/rspb.2002.2056)
20. Lopez P, Martin J. 2005 Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol. Lett. 1, 404-406. (doi:10. 1098/rsbl.2005.0360)
21. Ruther J, Matschke M, Garbe LA, Steiner S. 2009 Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis. Proc. R. Soc. B 276, 3303-3310. (doi:10.1098/rspb. 2009.0738)
22. Ilmonen P, Stundner G, Thoss M, Penn DJ. 2009 Females prefer the scent of outbred males: good-genes-as-heterozygosity? BMC Evol. Biol. 9, 104. (doi:10.1186/1471-2148-9-104)
23. Thom MD, Stockley P, Jury F, Ollier WER, Beynon RJ, Hurst JL. 2008 The direct assessment of genetic heterozygosity through scent in the mouse. Curr. Biol. 18, 619-623. (doi:10.1016/j.cub.2008.03.056)
24. Thoss M, Ilmonen P, Musolf K, Penn DJ. 2011 Major histocompatibility complex heterozygosity enhances reproductive success. Mol. Ecol. 20, 1546-1557. (doi:10.1111/j.1365-294X.2011.05009.x)
25. Pölkki M, Krams I, Kangassalo K, Rantala MJ. 2012 Inbreeding affects sexual signalling in males but not females of Tenebrio molitor. Biol. Lett. 8, 423-425. (doi:10.1098/rsbl.2011.1135)
26. Wyatt TD. 2009 Fifty years of pheromones. Nature 457, 262-263. (doi:10.1038/457262a)
27. van Oosterhout C, Zijlstra WG, van Heuven MK, Brakefield PM. 2000 Inbreeding depression and genetic load in laboratory metapopulations of the butterfly Bicyclus anynana. Evolution 54, 218-225.
28. Brakefield PM, Reitsma N. 1991 Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol. Entomol. 16, 291-303. (doi:10.1111/j.1365-2311.1991.tb00220.x)
29. Windig JJ, Brakefield PM, Reitsma N, Wilson JGM. 1994 Seasonal polyphenism in the wild: survey of wing patterns in 5 species of Bicyclus butterflies in Malawi. Ecol. Entomol. 19, 285-298. (doi:10.1111/j.1365-2311.1994.tb00420.x)
30. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I. 1998 Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491-494. (doi:10.1038/33136)
31. Costanzo K, Monteiro A. 2007 The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc. R. Soc. B 274, 845-851. (doi:10.1098/rspb.2006.3729)
32. Nieberding CM et al. 2008 The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis. PLoS ONE 3, e2751. (doi:10.1371/journal.pone.0002751)
33. Nieberding CM, Fischer K, Saastamoinen M, Allen CE, Wallin EA, Hedenström E, Brakefield PM. 2012 Cracking the olfactory code of a butterfly: the scent of ageing. Ecol. Lett. 15, 415-424. (doi:10.1111/j.1461-0248.2012.01748.x)
34. Brakefield PM, El Filali E, van der Laan R, Breuker CJ, Saccheri IJ, Zwaan B. 2001 Effective population size, reproductive success and sperm precedence in: the butterfly, Bicyclus anynana, in captivity. J. Evol. Biol. 14, 148-156. (doi:10.1046/j.1420-9101.2001. 00248.x)
35. van't Hof AE, Zwaan BJ, Saccheri IJ, Daly D, Bot ANM, Brakefield PM. 2005 Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana. Mol. Ecol. Notes 5, 169-172. (doi:10.1111/j.1471-8268.2005.00870.x)
36. Brakefield PM, Beldade P, Zwaan BJ. 2009 The African butterfly Bicyclus anynana: a model for evolutionary genetics and evolutionary developmental biology. In Emerging model organisms: a laboratory manual (eds R Behringer, A Johnson, R Krumlauf), pp. 291-329. Cold Spring Harbor, NY: CSHL Press.
37. Heuskin S, Godina B, Leroy P, Capella Q, Wathelet JP, Verheggen F, Haubruge E, Lognay G. 2009 Fast gas chromatography characterisation of purified semiochemicals from essential oils of Matricaria chamomilla L. (Asteraceae) and Nepeta cataria L. (Lamiaceae). J. Chromatogr. A 1216, 2768-2775. (doi:10.1016/j.chroma.2008.09.109)
38. Saastamoinen M, van der Sterren D, Vastenhout N, Zwaan BJ, Brakefield PM. 2010 Predictive adaptive responses: condition-dependent impact of adult nutrition and flight in the tropical butterfly Bicyclus anynana. Am. Nat. 176, 686-698. (doi:10.1086/657038)
39. DeRose MA, Roff DA. 1999 A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53, 1288-1292. (doi:10.2307/2640831)
40. Roff DA, Emerson K. 2006 Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60, 1981-1990. (doi:10.1111/j.0014-3820.2006.tb01836.x)
41. Kempenaers B. 2007 Mate choice and genetic quality: a review of the heterozygosity theory. Adv. Study Behav. 37, 189-278. (doi:10.1016/s0065- 83454(07)37005-8)
42. Whitlock MC, Agrawal AF. 2009 Purging the genome with sexual selection: reducing mutation load through selection on males. Evolution 63, 569-582. (doi:10.1111/j.1558-5646.2008.00558.x)
43. Roldan ERS, Cassinello J, Abaigar T, Gomendio M. 1998 Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc. R. Soc. Lond. B 265, 243-248. (doi:10.1098/rspb.1998.0288)
44. Gage MJG, Surridge AK, Tomkins JL, Green E, Wiskin L, Bell DJ, Hewitt GM. 2006 Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Curr. Biol. 16, 612-617. (doi:10.1016/j. cub.2006.02.059)
45. Dudley R. 2000 The biomechanics of insect flight: form, function, evolution. Princeton, NJ: Princeton University Press.
46. Berwaerts K, van Dyck H, Aerts P. 2002 Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct. Ecol. 16, 484-491. (doi:10.1046/j. 1365-2435.2002.00650.x)
47. Oostra V, de Jong MA, Invergo BM, Kesbeke F, Wende F, Brakefield PM, Zwaan BJ. 2011 Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly. Proc. R. Soc. B 278, 789-797. (doi:10. 1098/rspb.2010.1560)
48. Amrein H, Thorne N. 2005 Gustatory perception and behavior in Drosophila melanogaster. Curr. Biol. 15, R673-R684. (doi:10.1016/j.cub.2005.08.021)
49. Ebbs ML, Amrein H. 2007 Taste and pheromone perception in the fruit fly Drosophila melanogaster. Pflugers Arch. 454, 735-747. (doi:10.1007/s00424-007-0246-y)
50. Miyamoto T, Amrein H. 2008 Suppression of malecourtship by a Drosophila pheromone receptor. Nat. Neurosci. 11, 874-876. (doi:10.1038/nn.2161)
51. Lynch M, Walsh B. 1997 Genetics and the analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
52. Candolin U. 2003 The use of multiple cues in mate choice. Biol. Rev. 78, 575-595. (doi:10.1017/s1464793103006158)
53. Bretman A, Westmancoat James D, Gage Matthew JG, Chapman T. 2011 Males use multiple, redundant cues to detect mating rivals. Curr. Biol. 21, 617-622. (doi:10.1016/j.cub.2011.03.008)
54. Wyatt TD. 2003 Pheromones and animal behaviour: communication by smell and taste. New York, NY: Cambridge University Press.
55. Coleman SW. 2009 Taxonomic and sensory biases in the mate-choice literature: there are far too few studies of chemical and multimodal communication. Acta Ethol. 12, 45-48. (doi:10.1007/s10211-008-0050-5)
56. Campbell-Palmer R, Rosell F. 2011 The importance of chemical communication studies to mammalian conservation biology: a review. Biol. Conserv. 144, 1919-1930. (doi:10.1016/j.biocon.2011.04.028)