Sex-specific genotype-by-environment interactions for cuticular hydrocarbon expression in decorated crickets, Gryllodes sigillatus: Implications for the evolution of signal reliability

Journal of Evolutionary Biology

Volumn 25, Issue 10, 2012, Pages 2112-2125

  Weddle, C B ^a   Mitchell, C ^b   Bay, S K ^b   Sakaluk, S K ^a   Hunt, J ^b  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Chemical signals; Condition dependence; Cuticular hydrocarbons; Genotype by environment interaction; Gryllodes sigillatus; Individual recognition; Mate choice; Polyandry; Self referent phenotype matching; Sexual selection

Indexed keywords

HYDROCARBON;

CHEMICAL CUE; CONDITION FACTOR; CRICKET; CUTICLE; DIET; EVOLUTIONARY BIOLOGY; FOOD QUALITY; GENOTYPE-ENVIRONMENT INTERACTION; HYDROCARBON; LIFE HISTORY TRAIT; MATE CHOICE; NUTRITION; PHENOTYPIC PLASTICITY; POLYANDRY; RECOGNITION; SEXUAL SELECTION; SIGNAL;

ANIMAL; ARTICLE; DIET; ENVIRONMENT; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; GRYLLIDAE; INTEGUMENTARY SYSTEM; MALE; METABOLISM; NYMPH; PHYSIOLOGY; SEX DIFFERENCE;

ANIMALS; BIOLOGICAL EVOLUTION; DIET; ENVIRONMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOTYPE; GRYLLIDAE; HYDROCARBONS; INTEGUMENTARY SYSTEM; MALE; NYMPH; SEX FACTORS;

ANIMALIA; GRYLLIDAE; GRYLLODES SIGILLATUS;

EID: 84866174620     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02593.x     Document Type: Article

References (86)

1. Andersson, M. 1982. Sexual selection, natural selection and quality advertisement. Biol. J. Linn. Soc. 17: 373-393.
2. Andersson, M. 1986. Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40: 804-816.
3. Balakrishnan, R. & Pollack, G. 1997. The role of antennal sensory cues in female responses to courting males in the cricket Teleogryllus oceanicus. J. Exp. Biol. 200: 511-522.
4. Blomquist, G.J. & Jackson, L.L. 1973. Incorporation of labelled dietary n-alkanes into cuticular lipids of the grasshopper Melanoplus sanguinipes. J. Insect Physiol. 19: 1639-1647.
5. Blows, M.W., Chenoweth, S.F. & Hine, E. 2004. Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am. Nat. 163: 329-340.
6. Bussière, L.F., Hunt, J., Stolting, K.N., Jennions, M.D. & Brooks, R. 2008. Mate choice for genetic quality when environments vary: suggestions for empirical progress. Genetica 134: 69-78.
7. Chenoweth, S.F. & Blows, M.W. 2003. Signal trait sexual dimorphism and mutual sexual selection in Drosophila serrata. Evolution 57: 2326-2334.
8. Chenoweth, S.F. & Blows, M.W. 2005. Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata. Am. Nat. 165: 281-289.
9. Dale, J., Lank, D.B. & Reeve, H.K. 2001. Signaling individual identity versus quality: a model and case studies with ruffs, queleas, and house finches. Am. Nat. 158: 75-86.
10. Dani, F.R., Jones, G.R., Destri, S., Spencer, S.H. & Turillazzi, S. 2001. Deciphering the recognition signature within the cuticular chemical profile of paper wasps. Anim. Behav. 62: 165-171.
11. David, J.R., Gibert, P., Legout, H., Petavy, G., Capy, P. & Moreteau, B. 2005. Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94: 3-12.
12. Dietmann, V., Liebig, J., Holldobler, B. & Peeters, C. 2005. Changes in the cuticular hydrocarbons of incipient reproductives correlate with triggering of worker policing in the bulldog ant, Myrmecia gulcosa. Behav. Ecol. Sociobiol. 58: 486-496.
13. Elgar, M.A. & Allan, R.A. 2004. Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften 91: 143-147.
14. Falconer, D.S. & Mackay, T.F.C. 1996. Introduction to Quantitative Genetics, 4th edn. Longman Group Ltd., Harlow, UK.
15. Foley, B.R. & Telonis-Scott, M. 2011. Quantitative genetic analysis suggests causal association between cuticular hydrocarbon composition and desiccation survival in Drosophila melanogaster. Heredity 106: 68-77.
16. Gibbs, A.G. 1998. Water-proofing properties of cuticular lipids. Am. Zool. 38: 471-482.
17. Gibbs, A.G., Chippindale, A.K. & Rose, M.R. 1997. Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J. Exp. Biol. 200: 1821-1832.
18. Gosden, T.P. & Chenoweth, S.F. 2011. On the evolution of heightened condition dependence of male sexual displays. J. Evol. Biol. 24: 685-692.
19. Green, E.L. 1981. Genetics and Probability in Animal Breeding Experiments. Oxford University Press, New York, NY.
20. Greenfield, M.D. 2002. Signalers and Receivers: Mechanisms and Evolution of Arthropod Communication. Oxford University Press, New York, NY.
21. Greenfield, M.D. & Rodriguez, R.L. 2004. Genotype-environment interaction and the reliability of mating signals. Anim. Behav. 68: 1461-1468.
22. Haplin, Z.T. 1980. Individual odors and individual recognition: review and commentary. Biol. Behav. 5: 233-248.
23. Hauber, M.E. & Sherman, P.W. 2001. Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends Neurosci. 24: 609-616.
24. Herzner, G., Schmitt, T., Heckel, F., Schreier, P. & Strohm, E. 2006. Brothers smell similar: variation in the sex pheromone of male European Beewolves Philanthus triangulum F. (Hyme-noptera:Crabronidae) and its implications for inbreeding avoidance. Biol. J. Linn. Soc. 89: 433-442.
25. Higginson, A.D. & Reader, T. 2009. Environmental heterogeneity, genotype by environment interactions and the reliability of sexual traits as indicators of male quality. Proc. R. Soc. B 276: 1153-1159.
26. Hill, G.E. 2011. Condition-dependent traits as signals of functionality of vital cellular processes. Ecol. Lett. 14: 625-634.
27. Hine, E., Lachish, S., Higgie, M. & Blows, M.W. 2002. Positive genetic correlation between female preference and offspring fitness. Proc. R. Soc. Lond. B 269: 2215-2219.
28. Hine, E., Chenoweth, S.F. & Blows, M.W. 2004. Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions. Evolution 58: 2754-2762.
29. Holzer, B., Jacot, A. & Brinkhof, W.G. 2003. Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris. Behav. Ecol. 14: 353-359.
30. Hood, G.M. 2011. PopTools, version 3.2.5. URL http://www.poptools.org.
31. Howard, R.W. 1993. Cuticular hydrocarbons and chemical communication. In: Insect Lipids: Chemistry, Biochemistry and Biology (D.W. Stanley-Samuelson & D.R. Nelson, eds), pp. 179-226. University of Nebraska Press, Lincoln, NE.
32. Howard, R.W. & Blomquist, G.J. 1982. Chemical ecology and biochemistry of insect hydrocarbons. Annu. Rev. Entomol. 27: 149-172.
33. Howard, R.W. & Blomquist, G.J. 2005. Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu. Rev. Entomol. 50: 371-393.
34. Howard, R.W., McDaniel, C.A., Nelson, D.R., Blomquist, G.J., Gelbaum, L.T. & Zalkow, L.H. 1982. Cuticular hydrocarbons of Reticulitermes virginicus (Banks) and their role as potential species- and caste-recognition cues. J. Chem. Ecol. 8: 1227-1239.
35. Hunt, J., Brooks, R., Jennions, M.D., Smith, M.J., Bentsen, C.L. & Bussière, L.F. 2004a. High-quality male field crickets invest heavily in sexual display but die young. Nature 432: 1024-1027.
36. Hunt, J., Bussière, L.F., Jennions, M.D. & Brooks, R. 2004b. What is genetic quality? Trends Ecol. Evol. 19: 329-333.
37. Ingleby, F.C., Hunt, J. & Hosken, D.J. 2010. The role of genotype-by-environment interactions in sexual selection. J. Evol. Biol. 23: 2031-2045.
38. Ivy, T.M. 2007. Good genes, genetic compatibility and the evolution of polyandry: use of the diallel cross to address competing hypotheses. J. Evol. Biol. 20: 479-487.
39. Ivy, T.M. & Sakaluk, S.K. 2005. Polyandry promotes enhanced offspring survival in decorated crickets. Evolution 59: 152-159.
40. Ivy, T.M., Weddle, C.B. & Sakaluk, S.K. 2005. Females use self-referent cues to avoid mating with previous mates. Proc. R. Soc. B 272: 2475-2478.
41. Kirkpatrick, M. & Ryan, M.J. 1991. The evolution of mating preferences and the paradox of the lek. Nature 350: 33-38.
42. Liang, D. & Silverman, J. 2000. "You are what you eat": diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87: 412-416.
43. Liebert, A.E. & Starks, P.T. 2004. The action component of recognition systems: a focus on the response. Ann. Zool. Fenn. 41: 747-764.
44. Lockey, K.H. 1988. Lipids of the insect cuticle: origin, composition and function. Comp. Biochem. Physiol. B 89: 595-645.
45. Lynch, M. & Walsh, B. 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
46. Mateo, J.M. 2004. Recognition systems and biological organization: the perception component of social recognition. Ann. Zool. Fenn. 41: 729-745.
47. Moore, P., Reagan-Wallin, N., Haynes, K. & Moore, A. 1997. Odour conveys status on cockroaches. Nature 389: 25.
48. Nagamoto, J., Aonuma, H. & Hisada, M. 2005. Discrimination of conspecific individuals via cuticular pheromones by males of the cricket Gryllus bimaculatus. Zool Sci. 22: 1079-1088.
49. Narraway, C., Hunt, J., Wedell, N. & Hosken, D.J. 2010. Genotype-by-environment interactions for female preference. J. Evol. Biol. 23: 2550-2557.
50. 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.
51. Richard, F.-J., Hefetz, A., Christides, J.-P. & Errard, C. 2004. Food influence on colonial recognition and chemical signature between nestmates in the fungus-growing ant Acromyrmex subterraneus subterraneus. Chemoecology 14: 9-16.
52. Roff, D.A. & Preziosi, R. 1994. The estimation of the genetic correlation: the use of the jackknife. Heredity 73: 544-548.
53. Rowe, L. & Houle, D. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263: 1415-1421.
54. Rundle, H.D., Chenoweth, S.F., Doughty, P. & Blows, M.W. 2005. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol. 3: e368.
55. Ryan, K.M. & Sakaluk, S.K. 2009. Dulling the senses: the role of the antennae in mate recognition, copulation and mate guarding in decorated crickets. Anim. Behav. 77: 1345-1350.
56. Sakaluk, S.K. 1987. Reproductive behaviour of the decorated cricket, Gryllodes supplicans (Orthoptera: Gryllidae): calling schedules, spatial distribution, and mating. Behaviour 100: 202-225.
57. Sakaluk, S.K., Schaus, J.M., Eggert, A.K., Snedden, W.A. & Brady, P.L. 2002. Polyandry and fitness of offspring reared under varying nutritional stress in decorated crickets. Evolution 56: 1999-2007.
58. ® 9.1.3. SAS Institute, Inc., Cary, NC.
59. Scheuber, H., Jacot, A. & Brinkhof, M.W.G. 2003a. The effect of past condition on a multicomponent sexual signal. Proc. R. Soc. Lond. B 270: 1779-1784.
60. Scheuber, H., Jacot, A. & Brinkhof, M.W.G. 2003b. Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris. Anim. Behav. 65: 721-727.
61. Silverman, J. & Liang, D. 2001. Colony disassociation following diet partitioning in a unicolonial ant. Naturwissenschaften 88: 73-77.
62. Smith, R.L. & Thomas, W.B. 1988. Southwestern distribution and habitat ecology of Gryllodes supplicans. Bull. Entomol. Soc. Am. 34: 186-190.
63. Smith, J.M., Harper, D.G.C. & Brookfield, J.F.Y. 1988. The evolution of aggression: can selection generate variability? [and discussion]. Philos. Trans. R. Soc. Lond. B Biol. Sci. 319: 557-570.
64. Steiger, S., Peschke, K., Francke, W. & Muller, J.K. 2007. The smell of parents: breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorus vespilloides. Proc. R. Soc. B 274: 2211-2220.
65. Steiger, S., Peschke, K. & Muller, J.K. 2008. Correlated changes in breeding status and polyunsaturated cuticular hydrocarbons: the chemical basis of nestmate recognition in the burying beetle Nicrophorus vespilloides? Behav. Ecol. Sociobiol. 62: 1053-1060.
66. Stevens, J. 2002. Applied Multivariate Statistics for the Social Sciences, 4th edn. Lawrence Erlbaum Associates, Inc., Mahwah, NJ.
67. Tabachnick, B.G. & Fidell, L.S. 1998. Using Mulivariate Statistics, 2nd edn. Harper & Row, New York, NY.
68. Thom, M.D. & Hurst, J.L. 2004. Individual recognition by scent. Ann. Zool. Fenn. 41: 765-787.
69. Thomas, W.B. 1985. The distribution, biology, and management of the Indian house cricket Gryllodes supplicans. M.S. Thesis. Univeristy of Arizona, Tucson, Az.
70. Thomas, M.L. & Simmons, L.W. 2009a. Sexual selection on cuticular hydrocarbons in the Australian field cricket, Teleogryllus oceanicus. BMC Evol. Biol. 9: 162-174.
71. 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.
72. Thomas, M.L. & Simmons, L.W. 2011. Short-term phenotypic plasticity in long-chain cuticular hydrocarbons. Proc. R. Soc. B 278: 3123-3128.
73. Thomas, M.L., Gray, B. & Simmons, L.W. 2011. Male crickets alter the relative expression of cuticular hydrocarbons when exposed to different acoustic environments. Anim. Behav. 82: 49-53.
74. Tibbetts, E.A. & Curtis, T.R. 2007. Rearing conditions influence quality signals but not individual identity signals in Polistes wasps. Behav. Ecol. 18: 602-607.
75. Tibbetts, E.A. & Dale, J. 2004. A socially enforced signal of quality in a paper wasp. Nature 432: 218-222.
76. Tibbetts, E.A. & Dale, J. 2007. Individual recognition: it is good to be different. Trends Ecol. Evol. 22: 529-537.
77. Tolle, A.E. & Wagner, W.E. 2010. Costly signals in a field cricket can indicate high- or low-quality direct benefits, depending upon the environment. Evolution 65: 283-294.
78. Tomkins, J.L., Radwan, J., Kotiaho, J.S. & Tregenza, T. 2004. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19: 323-328.
79. Tregenza, T. & Wedell, N. 1997. Definitive evidence for cuticular pheromones in a cricket. Anim. Behav. 54: 979-984.
80. Van Homrigh, A., Higgie, M., McGuigan, K. & Blows, M.W. 2007. The depletion of genetic variance by sexual selection. Curr. Biol. 17: 528-532.
81. Via, S. & Lande, R. 1985. Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39: 505-522.
82. Via, S. & Lande, R. 1987. Evolution of genetic variability in a spatially heterogeneous environment: effects of genotype-environment interaction. Genet. Res. 49: 147-156.
83. Wagner, W.E. & Hoback, W.W. 1999. Nutritional effects on male calling behaviour in the variable field cricket. Anim. Behav. 57: 89-95.
84. Zahavi, A. 1975. Mate selection: a selection for a handicap. J. Theor. Biol. 53: 205-214.
85. Zahavi, A. 1977. The cost of honesty (further remarks on the handicap principle). J. Theor. Biol. 67: 603-605.
86. Zar, J.H. 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.