Experimental manipulation of sexual selection promotes greater male mating capacity but does not alter sperm investment

Evolution

Volumn 63, Issue 4, 2009, Pages 926-938

  Crudgington, Helen S ^a   Fellows, Sarah ^a   Badcock, Nichola S ^a   Snook, Rhonda R ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Accessory glands; Drosophila pseudoobscura; Experimental evolution; Relative testis mass; Sperm competition; Sperm heteromorphism

Indexed keywords

COMPETITION (ECOLOGY); EVOLUTIONARY BIOLOGY; FITNESS; FLY; MATING BEHAVIOR; PARENTAL INVESTMENT; REPRODUCTION; REPRODUCTIVE SUCCESS; SEXUAL SELECTION; SPERM;

ANIMAL; ARTICLE; BODY SIZE; DROSOPHILA; EVOLUTION; FEMALE; GENETIC SELECTION; HISTOLOGY; MALE; MATE CHOICE; ORGAN SIZE; PHYSIOLOGY; SPERMATOZOON;

ANIMALS; BODY SIZE; DROSOPHILA; EVOLUTION; FEMALE; MALE; MATING PREFERENCE, ANIMAL; ORGAN SIZE; SELECTION (GENETICS); SPERMATOZOA;

DROSOPHILA PSEUDOOBSCURA;

EID: 62749084985     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00601.x     Document Type: Article

References (71)

1. Anderson, W. W. 1974. Frequent multiple insemination in a natural population of Drosophila pseudoobscura. Am. Nat. 108 : 709 711.
2. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
3. Arnold, S. J. 1994. Bateman's principles and the measurement of sexual selection in plants and animals. Am. Nat. 144 : S126 S149.
4. Arnqvist, G., and T. Nilsson. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60 : 145 164.
5. Arnqvist, G., and L. Rowe. 2005. Sexual conflict. Princeton Univ. Press, Princeton, NJ.
6. Baayen, R. H. 2008. Analyzing linguistic data: a practical introduction to statistics using R. Cambridge Univ. Press, Cambridge, UK.
7. Bacigalupe, L., H. S. Crudgington, J. Slate, A. J. Moore, and R. R. Snook. 2008. Sexual selection and interacting phenotypes in experimental evolution: a study of Drosophila pseudoobscura mating behavior. Evolution 62 : 1804 1812.
8. Badcock, N. S. B. 2006. Reproductive conflict and sexual selection in insects. Ph.D. Thesis submitted to the Univ. of Sheffield, UK.
9. Baker, R. H., M. Denniff, P. Futerman, K. Fowler, A. Pomiankowski, and T. Chapman. 2003. Accessory gland size influences time to sexual maturity and mating frequency in the stalk-eyed fly, Cyrtodiopsis dalmanni. Behav. Ecol. 14 : 607 611.
10. Bangham, J., T. Chapman, and L. Partridge. 2002. Effects of body size, accessory gland and testis size on pre- and postcopulatory success in Drosophila melanogaster. Anim. Behav. 64 : 915 921.
11. Birkhead, T. R., and A. P. Møller. 1998. Sperm competition and sexual selection. Academic Press, London.
12. Birkhead, T. R., L. Atkin, and A. P. Møller. 1987. Copulation behaviour in birds. Behaviour 101 : 101 138.
13. Chapman, T. 2001. Seminal fluid-mediated fitness traits in Drosophila. Heredity 87 : 511 521.
14. Chen, P. S. 1984. The functional morphology and biochemistry of insect male accessory-glands and their secretions. Annu. Rev. Entomol. 29 : 233 255.
15. Crawley, M. J. 2007. The R book. John Wiley & Sons, Chichester, West Sussex.
16. Crudgington, H. S., A. P. Beckerman, L. Brustle, K. Green, and R. R. Snook. 2005. Experimental removal and elevation of sexual selection: does sexual selection generate manipulative males and resistant females? Am. Nat. 165 : S72 S87.
17. Dewsbury, D. A. 1982. Ejaculate cost and mate choice. Am. Nat. 119 : 601 610.
18. Dixon Scully, S. and M. E. Hellburg. 2006. Positive selection on nucleotide substitutions and indels in accessory gland proteins on the Drosophila pseudoobscura subgroup. J. Mol. Evol. 62 : 793 802.
19. Gilchrist, G. W., R. B. Huey, and L. Serra. 2001. Rapid evolution of wing size clines in Drosophila subobscura. Genetica 112 : 273 286.
20. Gomendio, M., A. H. Harcourt, and E. R. S. Roldan. 1998. Sperm competition in mammals. Pp. 667 756 in T. R. Birkhead and A. P. Møller, eds., Sperm competition and sexual selection. Academic Press, London.
21. Harcourt, A. H., P. H. Harvey, S. G. Larson, and R. V. Short. 1981. Testis weight, body weight and breeding system in primates. Nature 293 : 55 57.
22. Hihara, F. 1981. Effects of the male accessory gland secretion on ovipostion and remating in females of Drosophila melanogaster. Zoo. Mag. 90 : 307 316.
23. Holland, B., and W. R. Rice. 1999. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl. Acad. Sci. USA 96 : 5083 5088.
24. Holman, L., and R. R. Snook. 2006. Spermicide, cryptic female choice and the evolution of sperm form and function. J. Evol. Biol. 19 : 1660 1670.
25. Holman, L., and R. R. Snook. 2008. A sterile sperm caste protects brother fertile sperm from female-mediated death in Drosophila pseudoobscura. Curr. Biol. 18 : 292 296.
26. Holman, L., R. P. Freckleton, and R. R. Snook. 2008. What use is an infertile sperm? A comparative study of sperm-heteromorphic Drosophila. Evolution 62 : 374 385.
27. Hosken, D. J. 1997. Sperm competition in bats. Proc. R. Soc. Lond. B. 264 : 385 392.
28. Hosken, D. J., and P.I. Ward. 2001. Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4 : 10 13.
29. Hosken, D.J., T.W.J. Garner, and P.I. Ward. 2001. Sexual conflict selects for male and female reproductive characters. Curr. Biol. 11 : 489 493.
30. Kalb, J. M., A. J. DiBennedetto, and M. F. Wolfner. 1993. Probing the function of Drosophila accessory glands by directed cell ablation. Proc. Natl. Acad. Sci. USA 90 : 8093 8097.
31. Kotrba, M. 1996. Sperm transfer by spermatophore in Diptera: new results from the Diopsidae. Zool. J. Linn Soc. 117 : 305 323.
32. Lamunyon, C. W., and S. Ward. 1998. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc. R. Soc. Lond. B 265 : 1997 2002.
33. Linklater, J. R., B. Wertheim, S. Wigby, and T. Chapman. 2007. Ejaculate depletion patterns evolve in response to experimental manipulation of sex ratio in Drosophila melanogaster. Evolution 61 : 2027 2034.
34. Mueller, J. L., K. Rave Ram, L. A. McGraw, M. C. Bloch Qazi, E. D. Siggia, A. G. Clark, C. F. Aquadro, and M. F. Wolfner. 2005. Cross-species comparison of Drosophila male accessory gland protein genes. Genetics 171 : 131 143.
35. Parker, G. A. 1970a. Sperm Competition and its evolutionary consequences in the insects. Biol. Rev. 45 : 525 567.
36. Parker, G. A. 1970b. Sperm competition and its evolutionary effect on copula duration in the fly, Scatophaga stercoraria. J. Insect. Physiol. 16 : 1301 1328.
37. Parker, G. A. 1982. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J. Theor. Biol. 96 : 281 294.
38. Parker, G. A. 1984. Sperm competition and the evolution of animal mating strategies. Pp. 1 60 in R. L. Smith, ed., Sperm competition and the evolution of animal mating systems. Academic Press, London.
39. Parker, G. A. 1988. Sperm competition and the evolution of ejaculates: towards a theory base. Pp. 3 54 in T. R. Birkhead and A. P. Møller, eds., Sperm competition and sexual selection, Academic Press, London.
40. Parker, G. A. 1990. Sperm competition games - raffles and roles. Proc. R. Soc. Lond. B 242 : 120 126.
41. Pitnick, S., G. T. Miller, J. Reagan, and B. Holland. 2001a. Males' evolutionary responses to experimental removal of sexual selection. Proc. R. Soc. Lond. B 268 : 1071 1080.
42. Pitnick, S., W. D. Brown, and G. T. Miller. 2001b. Evolution of female remating behaviour following experimental removal of sexual selection. Proc. R. Soc. Lond. B 268 : 557 563.
43. Pizzari, T., and R. R. Snook. 2003. Sexual conflict and sexual selection: chasing away paradigm shifts. Evolution 57 : 1223 1236.
44. R Foundation for Statistical Computing. 2006. R: a language and environment for statistical computing and graphics. Available at http://www.r-project.org Accessed October 2008 Linklater, L. Lehmann, K. Fowler, T. Chapman, and G. D. D. Hurst. 2008. Adaptation to experimental alterations of the operational sex ratio in populations of Drosophila melanogaster. Evolution 62 : 401 412.
45. Ridley, M. 1988. Mating frequency and fecundity in insects. Biol. Rev. Camb. Philos. Soc. 63 : 509 549.
46. Robertson, F. W., and E. Reeve. 1952. Studies in quantitative inheritance 1. The effects of selection of wing and thorax length in Drosophila melanogaster. J. Genet. 50 : 414 448.
47. Rogers, D. W., H. H. Baker, T. Chapman, K. Fowler, M. Denniff, and A. Pomiankowski. 2005a. Direct and correlated responses to artificial selection on male mating frequency in the stalk-eyed fly Cyrtodopsis dalmanni. J. Evol. Biol. 18 : 642 650.
48. Rogers, D. W., T. Chapman, K. Fowler, and A. Pomiankowski. 2005b. Mating-induced reduction in accessory reproductive organ size in the stalk-eyed fly Cyrtodopsis dalmanni. BMC Evol. Biol. 5 : 36.
49. Rowe, L., E. Cameron, and T. Day. 2003. On detecting sexually antagonistic coevolution with population crosses. Proc. R. Soc. Lond. B 270 : 2009 2016.
50. Short, R. V. 1979. Sexual selection and component parts, somatic and genital selection, as illustrated by man and the great apes. Adv. Stud. Behav. 9 : 131 158.
51. Silberglied, R. E., J. G. Shepherd, and J. L. Dickinson. 1984. Eunuchs: the role of apyrene sperm in Lepidoptera. Am. Nat. 123 : 255 265.
52. Sivinski, J. 1984. Sperm in competition. Pp. 86 115 in R. L. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, London.
53. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton Univ. Press, Princeton NJ.
54. Simmons, L. W., and Siva-Jothy, M. T. 1998. Sperm competition in insects: mechanisms and the potential for selection. Pp. 341 434 in T. R. Birkhead and A. P. Møller, eds. Sperm competition and sexual selection. Academic Press, London.
55. Smith, R. L. 1984. Sperm competition and the evolution of animal mating systems. Academic Press Inc, Orlando.
56. Snook, R. R. 1997. Is the production of multiple sperm types adaptive? Evolution 51 : 797 808.
57. Snook, R. R. 1998. The risk of sperm competition and the evolution of sperm heteromorphism. Anim. Behav. 56 : 1497 1507.
58. Snook, R. R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20 : 46 53.
59. Snook, R.R., and T. A. Markow. 1996. Possible role of nonfertilizing sperm as a nutrient source for female Drosophila pseudoobscura Frolova (Diptera: Drosophilidae). Pan-Pacific Entomol. 72 : 121 129.
60. Snook, R. R., and T. A. Markow. 2002. Efficiency of gamete usage in nature: sperm storage, fertilization and polyspermy. Proc. R. Soc. Lond. B 269 : 467 473.
61. Snook, R. R., and T. L. Karr. 1998. Only long sperm are fertilization-competent in six sperm-heteromorphic Drosophila species. Curr. Biol. 8 : 291 294.
62. Snook, R. R., T. A. Markow, and T. L. Karr. 1994. Functional nonequivalence of sperm in Drosophila pseudoobscura. Proc. Natl. Acad. Sci. USA 91 : 11222 11226.
63. Snook, R. R., A. Robertson, H. S. Crudgington, and M.G. Ritchie. 2005. Experimental manipulation of sexual selection and the evolution of courtship song in Drosophila pseudoobscura. Behav. Gen. 35 : 245 255.
64. Stockley, P. 1997. Sexual conflict resulting from adaptations to sperm competition. Trends Ecol. Evol. 12 : 154 159.
65. Swallow, J. G., and G. S. Wilkinson. 2002. The long and short of sperm polymorphisms in insects. Biol. Rev. 77 : 153 182.
66. Till-Bottraud, I., D. Joly, D. Lachaise, and R. R. Snook. 2005. Pollen and sperm heteromorphism: convergence across kingdoms? J. Evol. Biol. 18 : 1 18.
67. Turner, M. E., and W. W. Anderson. 1984. Multiple mating and female fitness in Drosophila pseudoobscura. Evolution 37 : 714 723.
68. Wedell, N., M. J. G. Gage, and G. A. Parker. 2002. Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17 : 313 320.
69. Wigby, S., and T. Chapman. 2004. Female resistance to male harm evolves in response to manipulation of sexual selection. Evolution 58 : 1028 137.
70. Wolfner, M. F. 1997. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect. Biochem. Mol. Biol. 27 : 825 834.
71. Wolfner, M. F. 2002. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88 : 85 93.