Crickets detect the genetic similarity of mating partners via cuticular hydrocarbons

Journal of Evolutionary Biology

Volumn 24, Issue 8, 2011, Pages 1793-1800

  Thomas, Melissa L ^a   Simmons, L W ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Contact pheromones; Genetic compatibility; Inbreeding avoidance; Mate choice

Indexed keywords

HYDROCARBON;

CHEMICAL COMPOUND; CONSPECIFIC; CRICKET; FITNESS; GENETIC ANALYSIS; HYDROCARBON; INBREEDING AVOIDANCE; LIFE HISTORY TRAIT; MATE CHOICE; PHEROMONE; SENSORY SYSTEM;

ANIMAL; ANIMAL COMMUNICATION; ARTICLE; CHEMISTRY; FEMALE; GENETICS; GRYLLIDAE; MALE; MATE CHOICE; PHYSIOLOGY;

ANIMAL COMMUNICATION; ANIMALS; FEMALE; GRYLLIDAE; HYDROCARBONS; MALE; MATING PREFERENCE, ANIMAL;

ANIMALIA; ARTHROPODA; GRYLLIDAE; TELEOGRYLLUS OCEANICUS;

EID: 79960216926     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02319.x     Document Type: Article

References (69)

1. Balakrishnan, R. & Pollack, G.S. 1996. Recognition of courtship song in the field cricket, Teleogryllus oceanicus. Anim. Behav. 51: 353-366.
2. Beveridge, M. & Simmons, L.W. 2005. Microsatellite loci for the Australian field cricket Teleogryllus oceanicus and their cross-utility in Teleogryllus commodus. Mol. Ecol. Notes 5: 733-735.
3. Boulet, M., Charpentier, M. & Drea, C. 2009. Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate. BMC Evol. Biol. 9: 281.
4. Bowcock, A.M., Ruizlinares, A., Tomfohrde, J., Minch, E., Kidd, J.R. & Cavallisforza, L.L. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368: 455-457.
5. Bretman, A., Wedell, N. & Tregenza, T. 2004. Molecular evidence of post-copulatory inbreeding avoidance inthe field cricket Gryllus bimaculatus. Proc. Biol. Sci. 271: 159-164.
6. Bretman, A., Newcombe, D. & Tregenza, T. 2009. Promiscuous females avoid inbreeding by controlling sperm storage. Mol. Ecol. 18: 3340-3345.
7. Chapman, J.R., Nakagawa, S., Coltman, D.W., Slate, J. & Sheldon, B.C. 2009. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol. Ecol. 18: 2746-2765.
8. Charpentier, M.J.E., Boulet, M. & Drea, C.M. 2008. Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Mol. Ecol. 17: 3225-3233.
9. Charpentier, M.J.E., Crawford, J.C., Boulet, M. & Drea, C.M. 2010. Message 'scent': lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Anim. Behav. 80: 101-108.
10. Chertemps, T., Duportets, L., Labeur, C., Ueda, R., Takahashi, K., Saigo, K. et al. 2007. A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 104: 4273-4278.
11. Darwin, C. 1871. The Descent of Man, and Sexual Selection in Relation to Sex. John Murray, London.
12. Dronnet, S., Lohou, C., Christides, J.P. & Bagneres, A.G. 2006. Cuticular hydrocarbon composition reflects genetic relationship among colonies of the introduced termite Reticulitermes santonensis Feytaud. J. Chem. Ecol. 32: 1027-1042.
13. Evans, J.P. & Marshall, D.J. 2005. Male-by-female interactions influence fertilization success and mediates the benefits of polyandry in the sea urchin Heliocidaris erythogramma. Evolution 59: 106-112.
14. Ferveur, J.F. 2005. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35: 279-295.
15. Gillingham, M.A.F., Richardson, D.S., Løvlie, H., Moynihan, A., Worley, K. & Pizzari, T. 2009. Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proc. Biol. Sci. 276: 1083-1092.
16. Guo, S.W. & Thompson, E.A. 1992. Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48: 361-372.
17. Heth, G. & Todrank, J. 2000. Individual odour similarities across species parallel phylogenetic relationships in the S-ehrenbergi superspecies of mole-rats. Anim. Behav. 60: 789-795.
18. Jennions, M.D., Hunt, J., Graham, R. & Brooks, R. 2004. No evidence for inbreeding avoidance through postcopulatory mechanisms in the black field cricket, Teleogryllus commodus. Evolution 58: 2472-2477.
19. Kalinowski, S.T., Wagner, A.P. & Taper, M.L. 2006. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol. Ecol. Notes 6: 576-579.
20. Keller, L.F. & Waller, D.M. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17: 230-241.
21. Kempenaers, B. 2007. Mate choice and genetic quality: a review of the heterozygosity theory. Adv. Study Behav. 37: 189-278.
22. Kirkpatrick, M. & Ryan, M.J. 1991. The evolution of mating preferences and the paradox of the lek. Nature 350: 33-38.
23. Kotiaho, J.S., LeBas, N.R., Puurtinen, M. & Tomkins, J.L. 2008. On the resolution of the lek paradox. Trends Ecol. Evol. 23: 1-3.
24. Libersat, F., Murray, J.A. & Hoy, R.R. 1994. Frequency as a releaser in the courtship song of two crickets, Gryllus bimaculatus (de Geer) and Teleogryllus oceanicus: a neuroethological analysis. J. Comp. Physiol. 174: 485-494.
25. Lihoreau, M., Zimmer, C. & Rivault, C. 2008. Mutual mate choice: when it pays both sexes to avoid inbreeding. PLoS ONE 3: 7.
26. Loher, W. & Rence, B. 1978. The mating behaviour of Teleogryllus commodus (Walker) and its central and peripheral control. Z. Tierpsychol. 46: 225-259.
27. Mullen, S.P., Mendelson, T.C., Schal, C. & Shaw, K.L. 2007. Rapid evolution of cuticular hydrocarbons in a species radiation of acoustically diverse Hawaiian crickets (Gryllidae: Trigonidiinae: Laupala). Evolution 61: 223-231.
28. Nakagawa, S. & Cuthill, I.C. 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82: 591-605.
29. Neff, B.D. & Pitcher, T.E. 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol. 14: 19-38.
30. Parker, G.A. 2006. Sexual conflict over mating and fertilization: an overview. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361: 235-259.
31. Petfield, D., Chenoweth, S.F., Rundle, H.D. & Blows, M.W. 2005. Genetic variance in female condition predicts indirect genetic variance in male sexual display traits. Proc. Natl Acad. Sci. USA 102: 6045-6050.
32. Petrie, M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371: 598-599.
33. Pitcher, T.E. & Neff, B.D. 2006. MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon. Mol. Ecol. 15: 2357-2365.
34. Pizzari, T., Lovlie, H. & Cornwallis, C.K. 2004. Sex-specific, counteracting responses to inbreeding in a bird. Proc. R. Soc. Lond. B Biol. Sci. 271: 2115-2121.
35. Pusey, A. & Wolf, M. 1996. Inbreeding avoidance in animals. Trends Ecol. Evol. 11: 201-206.
36. Quinn, G.P. & Keogh, M.J. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
37. Reynolds, J.D. & Gross, M.R. 1992. Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proc. R. Soc. Lond. B 250: 57-62.
38. Rodriguez-Muñoz, R. & Tregenza, T. 2009. Genetic compatibility and hatching success in the sea lamprey (Petromyzon marinus). Biol. Lett. 5: 286-288.
39. Roelofs, W.L. & Rooney, A.P. 2003. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc. Natl Acad. Sci. USA 100: 9179-9184.
40. Roff, D.A. 1998. Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81: 28-37.
41. Roff, D.A. 2002. Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution 56: 768-775.
42. Roff, D.A. & DeRose, M.A. 2001. The evolution of trade-offs: effects of inbreeding on fecundity relationships in the cricket Gryllus firmus. Evolution 55: 111-121.
43. Sherborne, A.L., Thom, M.D., Paterson, S., Jury, F., Ollier, W.E.R., Stockley, P. et al. 2007. The genetic basis of inbreeding avoidance in house mice. Curr. Biol. 17: 2061-2066.
44. Simmons, L.W. 1986. Female choice in the field cricket, Gryllus bimaculatus (De Geer). Anim. Behav. 34: 1463-1470.
45. Simmons, L.W. 2010. Inbreeding depression in competitive fertilization success of male crickets. J. Evol. Biol. 24: 415-421.
46. Simmons, L.W. & Beveridge, M. 2010. The strength of postcopulatory sexual selection within natural populations of field crickets. Behav. Ecol. 21: 1179-1185.
47. Simmons, L.W. & Thomas, M.L. 2008. No postcopulatory response to inbreeding by male crickets. Biol. Lett. 4: 183-185.
48. Simmons, L.W., Beveridge, M., Wedell, N. & Tregenza, T. 2006. Postcopulatory inbreeding avoidance by female crickets only revealed by molecular markers. Mol. Ecol. 15: 3817-3824.
49. Stockley, P. 1999. Sperm selection and genetic incompatibility: does relatedness of mates affect male success in sperm competition? Proc. R. Soc. Lond. B Biol. Sci. 266: 1663-1669.
50. Takahashi, A., Tsaur, S.C., Coyne, J.A. & Wu, C.I. 2001. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 98: 3920-3925.
51. Thomas, M.L. 2011. Detection of female mating status using chemical signals and cues. Biol. Rev. 86: 1-13.
52. Thomas, M.L. & Simmons, L.W. 2008a. Cuticular hydrocarbons are heritable in the cricket Teleogryllus oceanicus. J. Evol. Biol. 21: 801-806.
53. Thomas, M.L. & Simmons, L.W. 2008b. Sexual dimorphism in cuticular hydrocarbons of the Australian field cricket Teleogryllus oceanicus (Orthoptera: Gryllidae). J. Insect Physiol. 54: 1081-1089.
54. Thomas, M.L. & Simmons, L.W. 2009a. Male derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets. Proc. Biol. Sci. 276: 383-388.
55. Thomas, M.L. & Simmons, L.W. 2009b. Male dominance influences pheromone expression, ejaculate quality, and fertilization success in the Australian field cricket, Teleogryllus oceanicus. Behav. Ecol. 20: 1118-1124.
56. Thomas, M.L. & Simmons, L.W. 2009c. Sexual selection on cuticular hydrocarbons in the Australian field cricket, Teleogryllus oceanicus. BMC Evol. Biol. 9: 162-173.
57. Thomas, M.L. & Simmons, L.W. 2010. Cuticular hydrocarbons influence female attractiveness to males in the Australian field cricket, Teleogryllus oceanicus. J. Evol. Biol. 23: 707-714.
58. Thomas, M.L. & Simmons, L.W. 2011. Short-term phenotypic plasticity in long-chain cuticular hydrocarbons. Proc. R. Soc. Lond. B, doi:.
59. Tomkins, J.L., Radwan, J., Kotiaho, J.S. & Tregenza, T. 2004. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19: 323-328.
60. Tregenza, T. & Wedell, N. 1997. Definitive evidence for cuticular pheromones in a cricket. Anim. Behav. 54: 979-984.
61. Tregenza, T. & Wedell, N. 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9: 1013-1027.
62. Tregenza, T. & Wedell, N. 2002. Polyandrous females avoid costs of inbreeding. Nature 415: 71-73.
63. Tsutsui, N.D., Suarez, A.V. & Grosberg, R.K. 2003. Genetic diversity, asymmetrical aggression, and cooperation in a widespread invasive species. Proc. Natl Acad. Sci. USA 100: 1078-1083.
64. Van Zweden, J.S., Brask, J.B., Christensen, J.H., Boomsma, J.J., Linksvayer, T.A. & D'Ettorre, P. 2010. Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. J. Evol. Biol. 23: 1498-1508.
65. Wicker-Thomas, C. & Chertemps, T. 2010. Molecular biology and genetics of hydrocarbon production. In: Insect Hydrocarbons; Biology, Biochemistry and Chemical Ecology (G.J. Blomquist & A.G. Bagnères, eds), pp. 53-74. Cambridge University Press, New York.
66. Willse, A., Belcher, A.M., Preti, G., Wahl, J.H., Thresher, M., Yang, P. et al. 2005. Identification of major histocompatibility complex-regulated body odorants by statistical analysis of a comparative gas chromatography/mass spectrometry experiment. Anal. Chem. 77: 2348-2361.
67. Willse, A., Kwak, J., Yamazaki, K., Preti, G., Wahl, J.H. & Beauchamp, G.K. 2006. Individual odortypes: interaction of MHC and background genes. Immunogenetics 58: 967-982.
68. Zeh, J.A. 1997. Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion. Behav. Ecol. Sociobiol. 40: 111-118.
69. Zeh, J.A. & Zeh, D.W. 1996. The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc. R. Soc. Lond. B 263: 1711-1717.