Opposing effects of sperm viability and velocity on the outcome of sperm competition

Behavioral Ecology

Volumn 23, Issue 4, 2012, Pages 820-826

  Smith, Chad C ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

alternative reproductive tactics; artificial insemination; Poeciliidae; sperm quality

Indexed keywords

FERTILIZATION (REPRODUCTION); LONGEVITY; MALE; REPRODUCTIVE STRATEGY; SPERM COMPETITION; TELEOST; TRADE-OFF;

POECILIIDAE; TELEOSTEI; XIPHOPHORUS NIGRENSIS;

EID: 84862905590     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/ars036     Document Type: Article

References (73)

1. Aitken JR, Roman DS. 2008. Antioxidative systems and oxidative stress in the testes. In: Cheng CY, editor. Molecular mechanisms in spermatogenesis. Advances in experimental medicine and biology. Austin: Landes Bioscience and Springer Science. p. 154-170.
2. Benson KE, Fox SF. 2007. Enhanced female brood patch size stimulates male courtship in Xiphophorus helleri. Copeia. 2007:212-217. (Pubitemid 46385772)
3. Birkhead TR, Martínez JG, Burke T, Froman DP. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B Biol Sci. 266:1759-1764. (Pubitemid 29433457)
4. Birkhead TR, Møller AP. 1998. Sperm competition and sexual selection. London: Academic Press.
5. Birkhead TR, Møller AP, Sutherland WJ. 1993. Why do females make it so difficult for males to fertilize their eggs? J Theor Biol. 161: 51-60.
6. Boschetto C, Gasparini C, Pilastro A. 2010. Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav Ecol Sociobiol. 65:813-821.
7. Brett BLH, Grosse DJ. 1982. A reproductive pheromone in the Mexican poeciliid fish Poecilia chica. Copeia. 1982:219-223.
8. Clark E. 1950. A method for artificial insemination in viviparous fishes. Science. 112:722-723.
9. Cornwallis CK, Birkhead TR. 2008. Plasticity in reproductive phenotypes reveals status-specific correlations between behavioral, morphological, and physiological sexual traits. Evolution. 62:1149-1161. (Pubitemid 351623933)
10. Crow RT, Liley NR. 1979. A sexual pheromone in the guppy, Poecilia reticulata (Peters). Can. J. Zool. 57:184-188.
11. delBarco-Trillo J. 2011. Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J Evol Biol. 24:1706-1714.
12. Den Boer SPA, Baer B, Boomsma JJ. 2010. Seminal fluid mediates ejaculate competition in social insects. Science. 327:1506-1509.
13. Dowling DK, Simmons LW. 2009. Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc Lond B Biol Sci. 276:1737-1745.
14. Dziminski MA, Roberts JD, Beveridge M, Simmons LW. 2009. Sperm competitiveness in frogs: slow and steady wins the race. Proc R Soc Lond B Biol Sci. 276:3955-3961.
15. Evans JP. 2010. Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proc R Soc Lond B Biol Sci. 277:1-7.
16. Evans JP, Zane L, Francescato S, Pilastro A. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Nature. 421:360-363. (Pubitemid 36157931)
17. Faraway JJ. 2006. Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. New York: Chapman & Hall/CRC.
18. Firman RC, Simmons LW. 2010. Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution. 64:1245-1256.
19. Froman D. 2003. Deduction of a model for sperm storage in the oviduct of the domestic fowl (Gallus domesticus). Biol Reprod. 69:248-253. (Pubitemid 36806829)
20. Fry CL, Wilkinson GS. 2004. Sperm survival in female stalk-eyed flies depends on seminal fluid and meiotic drive. Evolution. 58:1622.
21. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA. 2004. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol. 14:44-47. (Pubitemid 38069975)
22. Gage MJG, Morrow EH. 2003. Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Curr Biol. 13:754-757. (Pubitemid 36531023)
23. García-González F, Simmons LW. 2005. Sperm viability matters in insect sperm competition. Curr Biol. 15:271-275. (Pubitemid 40205710)
24. Gardiner DM. 1978. Utilization of extracellular glucose by spermatozoa of two viviparous fishes. Comp Biochem Phys. 59:165-168. (Pubitemid 8267407)
25. Gasparini C, Simmons LW, Beveridge M, Evans JP. 2010. Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS One. 5:1-5.
26. Gómez-Montoto L, Magaña C, Tourmente M, Martín-Coello J, Crespo C, Luque-Larena JJ, Gomendio M, Roldan ERS. 2011. Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS One. 6:e18173.
27. Greven H. 2011. Gonads, genitals, and reproductive biology. In: Evans JP, Pilastro A, Schlupp I, editors. Ecology and evolution of Poeciliid fishes. Chicago (IL): Chicago University Press. p. 3-19.
28. Hosken DJ, Ward PI. 2001. Experimental evidence for testis size evolution via sperm competition. Ecol Lett. 4:10-13. (Pubitemid 32145264)
29. Houde AE. 1997. Sex, color and mate choice in guppies. Princeton (NJ): Princeton University Press.
30. Hunter FM, Birkhead TR. 2002. Sperm viability and sperm competition in insects. Curr Biol. 12:121-123. (Pubitemid 34099135)
31. Kallman KD. 1989. Genetic control of size at maturity in Xiphophorus. In: Meffe GK, Snelson FF, editors. Ecology and evolution of livebearing fishes (Poeciliidae). Englewood Cliffs (NJ): Prentice Hall. p. 163-184.
32. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT. 2009. Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution. 63:2466-2473.
33. Lampert KP, Schmidt C, Fischer P, Volff J-N, Hoffmann C, Muck J, Lohse MJ, Ryan MJ, Schartl M. 2010. Determination of onset of sexual maturation and mating behavior by melanocortin receptor 4 polymorphisms. Curr Biol. 20:1729-1734.
34. Levitan DR. 2000. Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc Lond B Biol Sci. 267:531-534. (Pubitemid 30175488)
35. Liley NR. 1966. Ethological isolating mechanisms in four sympatric species of poeciliid fishes. Behaviour. 13:1-197.
36. Manier MK, Belote JM, Berben KS, Novikov D, Stuart WT, Pitnick S. 2010. Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science. 328:354-357.
37. Morisawa M, Suzuki K. 1980. Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science. 210:1145-1147. (Pubitemid 11166027)
38. Mortimer D, Pandya IJ, Sawers RS. 1986. Relationship between human sperm motility characteristics and sperm penetration into human cervical mucus in vitro. J Reprod Fertil. 78:93-102. (Pubitemid 16050378)
39. Nakagawa S, Cuthill IC. 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev. 82:591-605. (Pubitemid 47609922)
40. Parker GA. 1970. Sperm competition and its evolutionary consequences in the insects. Biol Rev. 45:525-567.
41. Parker GA. 1990a. Sperm competition games-sneaks and extra-pair copulations. Proc R Soc Lond B Biol Sci. 242:127-133.
42. Parker GA. 1990b. Sperm competition games-raffles and roles. Proc R Soc Lond B Biol Sci. 242:120-126.
43. Parker GA. 1993. Sperm competition games-sperm size and sperm number under adult control. Proc R Soc Lond B Biol Sci. 253:245-254.
44. Peden AE. 1973. Variation in anal spot expression of Gambusiin females and its effect on male courtship. Copeia. 1973:250-263.
45. Pitnick S, Miller GT, Reagan J, Holland B. 2001. Males' evolutionary responses to experimental removal of sexual selection. Proc R Soc Lond B Biol Sci. 268:1071-1080. (Pubitemid 32500481)
46. Pitnick S, Wolfner MF, Suarez SS. 2009. Ejaculate-female and spermfemale interactions. In: Birkhead TR, Hosken DJ, Pitnick SS, editors. Sperm biology: an evolutionary perspective. 1st ed. London: Academic Press. p. 247-304.
47. Pizzari T, Dean R, Pacey A, Moore H, Bonsall MB. 2008. The evolutionary ecology of pre-and post-meiotic sperm senescence. Trends Ecol Evol. 23:131-140.
48. Pizzari T, Parker GA. 2009. Sperm competition and the sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick SS, editors. Sperm biology: an evolutionary perspective. 1st ed. London: Academic Press. p. 207-245.
49. Pizzari T, Worley K, Burke T, Froman D. 2008. Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol Biol. 8:332.
50. Potter H, Kramer CR. 2000. Ultrastructural observations on sperm storage in the ovary of the platyfish, Xiphophorus maculatus (Teleostei: poeciliidae): the role of the duct epithelium. J Morphol. 245:110-129. (Pubitemid 30608934)
51. R Development Core Team. 2010. R: a language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing. [cited 2012 March 5]. Available from: http://www.R-project.org.
52. Ramsey ME, Wong RY, Cummings ME. 2011. Estradiol, reproductive cycle and preference behavior in a northern swordtail. Gen Comp Endocrin. 170:381-390.
53. Reinhardt K. 2007. Evolutionary consequences of sperm cell aging. Q Rev Biol. 82:375-393. (Pubitemid 351412253)
54. Reznick DN, Miles DB. 1989. A review of life history patterns in poeciliid fishes. In: Meffe GK, Snelson FF, editors. Ecology and evolution of livebearing fishes (Poeciliidae). Prentice Hall advanced reference series. Physical and life sciences. Englewood Cliffs (NJ): Prentice Hall. p. 125-148.
55. Rowe M, Pruett-Jones S. 2011. Sperm competition selects for sperm quantity and quality in the Australian Maluridae. PLoS One. 6:e15720.
56. Ryan MJ, Causey BA. 1989. Alternative mating behavior in the swordtails Xiphophorus nigrensis and Xiphophorus pygmaeus (Pisces, Poeciliidae). Behav Ecol Sociobiol. 24:341-348.
57. Sherman CD, Wapstra E, Uller T, Olsson M. 2008. Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii. Proc R Soc Lond B Biol Sci. 275:971-978. (Pubitemid 351323638)
58. Sherman CDH, Wapstra E, Olsson M. 2009. Consistent male-male paternity differences across female genotypes. Biol Lett. 5:232-234.
59. Siciliano MJ. 1972. Evidence for a spontaneous ovarian cycle in fish of the genus Xiphophorus. Biol Bull. 142:480-488.
60. Simmons LW, Beveridge M. 2011. Seminal fluid affects sperm viability in a cricket. PLoS One. 6:e17975.
61. Simmons LW, García-González F. 2008. Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution. 62:2580-2591.
62. Simmons LW, Moore SS. 2009. Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick SS, editors. Sperm biology: an evolutionary perspective. 1st ed. London: Academic Press. p. 405-434.
63. Simmons LW, Wernham J, García-González F, Kamien D. 2003. Variation in paternity in the field cricket Teleogryllus oceanicus: no detectable influence of sperm numbers or sperm length. Behav Ecol. 14:539-545. (Pubitemid 37042026)
64. Smith CC. 2011. Sperm competition and the evolution of alternative reproductive tactics in the swordtail Xiphophorus nigrensis [PhD dissertation] [Internet]. Austin (TX): University of Texas at Austin. [cited 2012 March 5]. Available from: https://repositories.lib.utexas.edu/bitstream/handle/2152/ETD- UT-2011-05-3128/SMITH-DISSER TATION.pdf.
65. Smith CC, Ryan MJ. 2010. Evolution of sperm quality but not quantity in the internally fertilized fish Xiphophorus nigrensis. J Evol Biol. 17:1759-1771.
66. Smith CC, Ryan MJ. 2011. Tactic-dependent plasticity in ejaculate traits in the swordtail Xiphophorus nigrensis. Biol Lett. 7:733-735.
67. Snook RR. 2005. Sperm in competition: not playing by the numbers. Trends Ecol Evol. 20:46-53. (Pubitemid 40078228)
68. Suarez SS, Pacey AA. 2006. Sperm transport in the female reproductive tract. Hum Reprod Update. 12:23-37. (Pubitemid 43013744)
69. Venables WN, Ripley BD. 2002. Modern applied statistics with S. 4th ed. New York: Springer. Available from: http://www.stats.ox.ac. uk/pub/MASS4.
70. Wang J, Santure AW. 2009. Parentage and sibship inference from multilocus genotype data under polygamy. Genetics. 181: 1579-1594.
71. Wedell N, Gage MJG, Parker GA. 2002. Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol. 17: 313-320. (Pubitemid 34628657)
72. Wilson-Leedy JG, Ingermann RL. 2007. Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology. 67: 661-672. (Pubitemid 46026865)
73. World Health Organization. 1999. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. Cambridge: Cambridge University Press.