Advertisement

Behavioral Ecology and Sociobiology

, Volume 35, Issue 4, pp 235–241 | Cite as

Genetic evidence for the “good genes” process of sexual selection

  • A. J. Moore
Article

Abstract

The adaptive nature of female mate choice remains one of the most contentious issues in the study of sexual selection. Here, I provide evidence that mate choice by females of the ovoviviparous cockroach Nauphoeta cinerea influences the rate at which offspring develop and provides both direct and indirect benefits to the female. Males that are more attractive to females produce offspring with shorter development times than less preferred males. Development time is heritable and apparently unconstrained by antagonistic pleiotropy. Male attractiveness and rate of offspring development are genetically correlated. Offspring gain an indirect benefit from their mother's mate choice because, on average, individuals that hatch faster reach sexual maturity more quickly. Females that discriminate among males gain a direct benefit because N. cinerea is ovoviviparous and the time between clutches is decreased by producing offspring with shorter development. In addition to providing evidence for beneficial consequences of mate choice, this study highlights how genetic data provide insights into the process of sexual selection not gained in a purely phenotypic study.

Key words

Female mate choice Offspring development time Heritability Direct and indirect benefits Nauphoeta cinerea Genetic correlations 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arnold SJ (1985) Quantitative genetic models of sexual selection. Experientia 41: 1296–1310Google Scholar
  2. Arnold SJ, Houck LD (1982) Courtship pheromones: evolution by natural and sexual selection. In: Nitecke M (ed) Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago, pp 173–211Google Scholar
  3. Baker TC, Cardé RT (1979) Courtship behavior of the oriental fruit moth (Grapholitha molesta): experimental analysis and consideration of the role of sexual selection in the evolution of courtship pheromones in the Lepidoptera. Ann Entomol Soc Am 72: 173–188Google Scholar
  4. Bateson P (ed) (1983) Mate choice. Cambridge University Press, CambridgeGoogle Scholar
  5. Becker WA (1984) Manual of quantitative genetics, 4th edn. Academic Enterprises, Pullman, WashingtonGoogle Scholar
  6. Bell WJ, Gorton RE (1978) Informational analysis of agonistic behaviour and dominance hierarchy formation in a cockroach, Nauphoeta cinerea. Behaviour 67: 217–235Google Scholar
  7. Boake CRB ( 1985) Genetic consequences of mate choice: a quantitative genetic method for testing sexual selection theory. Science 227: 1061–1063Google Scholar
  8. Boake CRB (1986) A method for testing adaptive hypotheses of mate choice. Am Nat 127: 654–666Google Scholar
  9. Bradbury JW, Andersson MB (1987) Sexual selection: testing the alternatives. Wiley, New YorkGoogle Scholar
  10. Breed MD, Smith SK, Gall BG (1980) Systems of mate selection in a cockroach species with male dominance hierarchies. Anim Behav 28: 130–134Google Scholar
  11. Brossut R, Dubois P, Rigaud J, Sreng L (1975) Etude biochimique de la secretion des glandes tergales des Blattaria. Insect Biochem 5: 719–732Google Scholar
  12. Butlin RK, Hewitt GM (1986) Heritability estimates for characters under sexual selection in the grasshopper, Chorthippus brunneus. Anim Behav 34: 1256–1261Google Scholar
  13. Cheverud JM (1984) Evolution by kin selection: a quantitative genetic model illustrated by maternal performance in mice. Evolution 38: 766–777Google Scholar
  14. Cheverud JM, Moore AJ (1994) Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In: Boake CRB (ed) Quantitative genetic analyses of behavioral evolution. University of Chicago Press, Chicago, pp 67–100Google Scholar
  15. Conner WE, Eisner T, Vander Meer RK, Guerrero A, Meinwald J (1981) Precopulatory sexual interaction in an arctiid moth (Utetheisa ornatrix): the role of a pheromone derived from dietary alkaloids. Behav Ecol Sociobiol 9: 227–235Google Scholar
  16. Darwin CR (1871) The descent of man and selection in relation to sex. John Murray, LondonGoogle Scholar
  17. Eisen EJ (1967) Mating designs for estimating direct and maternal genetic variances and direct-maternal covariances. Can J Genet Cytol 9: 13–22Google Scholar
  18. Ewing LS (1972) Hierarchy and its relation to territoriality in the cockroach Nauphoeta cinerea. Behaviour 42: 152–173Google Scholar
  19. Ewing LS (1973) Territoriality and the influence of females on the spacing of males in the cockroach Nauphoeta cinerea. Behaviour 45: 281–304Google Scholar
  20. Ewing LS, Ewing AW (1973) Correlates of subordinate behaviour in the cockroach, Nauphoeta cinerea. Anim Behav 21: 571–578Google Scholar
  21. Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Wiley, New YorkGoogle Scholar
  22. Fisher RA (1915) The evolution of sexual preference. Eugen Rev 7: 184–192Google Scholar
  23. Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New YorkGoogle Scholar
  24. Fukui M, Takahashi S (1983) Studies on the mating behavior of the cockroach Nauphoeta cinerea (Olivier) (Dictyoptera: Blaberidae) III. Isolation and identification of intermale recognition pheromone. Appl Entomol Zool 18: 351–356Google Scholar
  25. Hedrick AV (1988) Female choice and the heritability of attractive male traits: an empirical study. Am Nat 132: 267–276Google Scholar
  26. Heisler IL (1994) Quantitative genetic models of the evolution of mating behavior. In: Boake CRB (ed) Quantitative genetic analyses of behavioral evolution. University of Chicago Press, Chicago, pp 101–125Google Scholar
  27. Heywood JS (1989) Sexual selection by the handicap mechanism. Evolution 43: 1387–1397Google Scholar
  28. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350: 337–339Google Scholar
  29. Houde AE (1992) Sex-linked heritability of a sexually selected character in a natural population of Poecilia reticulata (Pisces: Poeciliidae) (guppies). Heredity 69: 229–235Google Scholar
  30. Kirkpatrick M (1987) Sexual selection by female choice in polygynous animals. Annu Rev Ecol Syst 18: 43–70Google Scholar
  31. Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43: 485–503Google Scholar
  32. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350: 33–38Google Scholar
  33. Lande R, Kirkpatrick M (1990) Selection response in traits with maternal inheritance. Genet Res Camb 55: 189–197Google Scholar
  34. Lynch M (1987) Evolution of intrafamilial interactions. Proc Natl Acad Sci USA 84: 8507–8511Google Scholar
  35. Manly BFJ (1991) Randomization and Monte Carlo methods in biology. Chapman and Hall, LondonGoogle Scholar
  36. Maynard Smith J (1991) Theories of sexual selection. Trends Ecol Evol 6: 146–151Google Scholar
  37. McLain DK (1987) Heritability of size, a sexually selected character, and the response to sexual selection in a natural population of the southern green stink bug, Nezara viridula (Hemiptera: Pentatomidae). Heredity 59: 391–395Google Scholar
  38. Menon M (1981) Morphological evidence for probable secretory site for the pheromone “seducin” in males of Nauphoeta cinerea. I. Light microscope studies. J Morphol 168: 229–237Google Scholar
  39. Menon M (1986) Morphological evidence for probable secretory site of the male sex pheromones of Nauphoeta cinerea (Blateria, Blaberidae). 2. Electron microscope studies. J Morphol 187: 69–79Google Scholar
  40. Møller AP (1991) Viability is positively related to degree of ornamentation in male swallows. Proc R Soc Lond B 243: 145–148Google Scholar
  41. Moore AJ (1988) Female preferences, male social status, and sexual selection in Nauphoeta cinerea. Anim Behav 36: 303–305Google Scholar
  42. Moore AJ (1990a) The inheritance of social dominance, mating behaviour and attractiveness to mates in male Nauphoeta cinerea. Anim Behav 39: 388–397Google Scholar
  43. Moore AJ (1990b) Sexual selection and the genetics of pheromonally mediated social behavior in Nauphoeta cinerea (Dictyoptera: Blaberidae). Entomol Gener 15: 133–147Google Scholar
  44. Moore AJ, Breed MD (1986) Mate assessment in a cockroach, Nauphoeta cinerea. Anim Behav 34: 1160–1164Google Scholar
  45. Moore AJ, Moore PJ (1988) Female strategy during mate choice: threshold assessment. Evolution 42: 387–391Google Scholar
  46. Moore AJ, Reagan NR, Haynes KF (in press) Conditional signalling strategies: effects of ontogeny, social experience, and social status on the pheromonal signal of male cockroaches, Nauphoeta cinerea. Anim Behav (in press)Google Scholar
  47. Mullins DE, Kiel CB (1980) Paternal investment of urates in cockroaches. Nature 283: 567–569Google Scholar
  48. Norris K (1993) Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362: 537–539Google Scholar
  49. O'Donald P (1990) Fisher's contributions to the theory of sexual selection as the basis of recent research. Theor Popul Biol 38: 285–300Google Scholar
  50. Petrie M, Williams A (1993) Peahens lay more eggs for peacocks with larger trains. Proc R Soc Lond B 251: 127–131Google Scholar
  51. Phelan PL, Baker TC (1986) Male-size related courtship success in intersexual selection in the tobacco moth, Ephestia elutella. Experientia 42: 1291–1293Google Scholar
  52. Pomiankowski AN (1988) The evolution of female mate preferences for male genetic quality. Oxford Surv Evol Biol 5: 136–184Google Scholar
  53. Price T, Schluter D, Heckman NE (1993) Sexual selection when the female directly benefits. Biol J Linn Soc 48: 187–211Google Scholar
  54. Roth LM (1962) Hypersexual activity induced in females of the cockroach Nauphoeta cinerea. Science 138: 1267–1269Google Scholar
  55. Roth LM (1964a) Control of reproduction in female cockroaches with special reference to Nauphoeta cinerea. I. First pre-oviposition period. J Insect Physiol 10: 915–945Google Scholar
  56. Roth LM (1964b) Control of reproduction in female cockroaches with special reference to Nauphoeta cinerea. II. Gestation and postparturition. Psyche 71: 198–244Google Scholar
  57. Roth LM (1967) Uricose glands in the accessory sex gland complex of male Blattaria. Ann Entomol Soc Am 60: 1203–1211Google Scholar
  58. Roth LM, Barth RH (1967) The sense organs employed by cockroaches in mating behavior. Behaviour 28:58–94Google Scholar
  59. Roth LM, Dateo GP (1966) A sex pheromone produced by males of the cockroach Nauphoeta cinerea. J Insect Physiol 12:255–265Google Scholar
  60. Roth LM, Hahn W (1964) Size of new-born larvae of cockroaches incubating eggs internally. J Insect Physiol 10:65–72Google Scholar
  61. Roth LM, Willis ER (1958) An analysis of oviparity and viviparity in the Blatteria. Trans Am Entomol Soc 83:221–238Google Scholar
  62. Schal C, Bell WJ (1983) Determinants of dominant-subordinate interactions in males of the cockroach Nauphoeta cinerea. Biol Behav 8:117–139Google Scholar
  63. Simmons LW (1987a) Female choice contributes to offspring fitness in the field cricket, Gryllus bimaculatus (De Geer). Behav Ecol Sociobiol 21:313–321Google Scholar
  64. Simmons LW (1987b) Heritability of a male character chosen by females of the field cricket, Gryllus bimaculatus. Behav Ecol Sociobiol 21:129–133Google Scholar
  65. Sirugue D, Bonnard O, LeQuere J-L, Farine J-P, Brossut R (1992) 2-methylthiazolidine and 4-ethylguaiacol, male sex pheromone components of the cockroach Nauphoeta cinerea (Dictyoptera, Blaberidae): a reinvestigation. J Chem Ecol 18:2261–2276Google Scholar
  66. Smith SK, Breed MD (1982) Olfactory cues in discrimination among individuals in dominance hierarchies in the cockroach, Nauphoeta cinerea. Physiol Entomol 7:337–341Google Scholar
  67. Sreng L (1984) Morphology of the sternal and tergal glands producing the sexual pheromones and the aphrodisiacs among the cockroaches of the subfamily Oxyhaloinae. J Morphol 182:279–284Google Scholar
  68. Sreng L (1985) Ultrastructure of the glands producing sex pheromones of the male Nauphoeta cinerea (Insecta: Dictyoptera). Zoomorphology 105:133–142Google Scholar
  69. Sreng L (1990) Seducin, male sex pheromone of the cockroach Nauphoeta cinerea: isolation, identification, and bioassay. J Chem Ecol 16:2899–2912Google Scholar
  70. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, CambridgeGoogle Scholar
  71. Von Schantz T, Göransson G, Andersson G, Fröberg I, Grahn, M, Helgée A, Wittzell H (1989) Female choice selects for a viability-based male trait in pheasants. Nature 337: 166–169Google Scholar
  72. Willis ER, Riser GR, Roth LM (1958) Observations on reproduction and development in cockroaches. Ann Entomol Soc Am 51: 53–59Google Scholar
  73. Williams GC (1992) Natural selection. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • A. J. Moore
    • 1
  1. 1.Department of Entomology, Center for Ecology, Evolution, and BehaviorUniversity of KentuckyLexingtonUSA

Personalised recommendations