Abstract
Ovulation generally takes two forms: spontaneous and induced. These two ovulatory modes are predicted to cause different levels of male–male competition due to differences in males’ ability to predict the timing of ovulation of females that use each mode. Ovulation mode has been shown to be correlated with differences in testis size, but it is not known whether ovulation type influences ejaculate traits, specifically sperm quantity (sperm concentration, ejaculate volume, total motile sperm per ejaculate) and/or sperm quality (% sperm motility, % normal sperm). Using a cross-species comparative analysis of 130 mammals, we found that sperm concentration and total motile sperm per ejaculate were significantly greater in spontaneous ovulators. In contrast, ejaculate volume, % sperm motility and % normal sperm were unrelated to ovulation type. These data show that ovulation alters sperm quantity by increasing sperm concentration but not ejaculate volume, and that sperm quality does not vary with ovulation mode.
Similar content being viewed by others
References
Adams GP, Ratto MH, Huanaca W, Singh J (2005) Ovulation-inducing factor in the seminal plasma of alpacas and llamas. Biol Reprod 73:452–457
Anderson MJ, Dixson AF (2002) Sperm competition: motility and the midpiece in primates. Nature 416:496
Anderson MJ, Nyholt J, Dixson AF (2005) Sperm competition the evolution of sperm midpiece volume in mammals. J Zool 267:135–142
Anderson MJ, Dixson AS, Dixson AF (2006) Mammalian sperm and oviducts are sexually selected: evidence for co-evolution. J Zool 270:682–686
Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512
Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2008) Corrigendum. Nature 456:274
Birkhead TR (1999) The role of sperm competition in reproduction. In: Glover TD, Barratt LR (eds) Male fertility and infertility. Cambridge University Press, Cambridge, pp 18–33
Birkhead T (2000) Promiscuity. Faber and Faber, London
Cameron E, Day T, Rowe L (2007) Sperm competition and the evolution of ejaculate composition. Am Nat 169:E158–E172
Cohen J (1973) Cross-overs, sperm redundancy and their close association. Hered 31:408–413
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Erlbaum, Hillsdale, p 567
Conaway CH (1971) Ecological adaptation and mammalian reproduction. Biol Reprod 4:239–247
Dewsbury DA (1984) Sperm competition in muroid rodents. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, New York, pp 547–571
Dott H, Glover T (1999) Sperm production and delivery in mammals, including man. In: Glover TD, Barratt LR (eds) Male fertility and infertility. Cambridge, Cambridge University Press, pp 34–55
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
Eberhard WG (1998) Female roles in sperm competition. In: Birkhead TR, Møller AP (eds) Sperm Competition and Sexual Selection. Academic Press, London, pp 91–118
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Freckleton RP (2009) The seven deadly sins of comparative analysis. J Evol Biol 22:1367–1375
Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726
Gage MJG (1994) Association between body size, mating pattern, testis size and sperm length across butterflies. Proc R Soc Lond B 258:247–254
Gage MJG, Freckleton RP (2003) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc Lond B 270:625–632
Gage MJG, Surridge AK, Tomkins JL, Green E, Wiskin L, Bell DJ, Hewitt GM (2006) Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Curr Biol 16:612–617
Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184
Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc Lond B 243:181–185
Gomendio M, Harcourt AH, Roldán ERS (1998) Sperm competition in mammals. In: Birkhead TR, Møller AP (eds) Sperm Competition and Sexual Selection. Academic Press, London, pp 667–755
Harcourt AH (1991) Sperm competition and the evolution of nonfertilizing sperm in mammals. Evolution 45:314–328
Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testis weight body weight and breeding system in primates. Nature 93:55–57
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford
Hosken DJ, Ward PI (2001) Experimental evidence for testis size evolution via sperm competition. Ecol Lett 4:10–13
Hunter FM, Birkhead TR (2002) Sperm viability and sperm competition in insects. Curr Biol 12:121–123
Iossa G, Soulsbury CD, Baker PJ, Harris S (2008) Sperm competition and the evolution of testes size in terrestrial mammalian carnivores. Funct Ecol 22:655–662
Isvaran K, Clutton-Brock TH (2007) Ecological correlates of extra-group paternity in mammals. Proc R Soc B 274:219–224
Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mammal 67:1–22
Møller AP (1988a) Testes size, ejaculate quality and sperm competition in birds. Biol J Linn Soc 33:273–283
Møller AP (1988b) Ejaculate quality, testis size and sperm competition in primates. J Hum Evol 17:479–488
Møller AP (1989) Ejaculate quality, testes size and sperm production in mammals. Funct Ecol 3:91–96
Møller AP (1991) Concordance of mammalian ejaculate features. Proc R Soc Lond B 246:237–241
Moore HDM, Martin M, Birkhead TR (1999) No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proc Roy Soc Lond B 266:2343–2350
Moore PJ, Harris WE, Montrose VT, Levin D, Moore AJ (2004) Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58:1773–1780
Morato RG, Conforti VA, Azevedo FC, Jacomo AT, Silveira L, Sana D, Nunes AL, Guimaraes MA, Barnabe RC (2001) Comparative analyses of semen and endocrine characteristics of free-living versus captive jaguars (Panthera onca). Reprod 122:745–751
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605
Ostner J, Nunn CL, Schülke O (2008) Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19:1150–1158
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567
Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, New York, pp 2–60
Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 1–49
Pizzari T, Parker GA (2008) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm Biology. An evolutionary perspective. Academic Press, Oxford, pp 207–245
Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289–310
Purvis AA (1995) Composite estimate of primate phylogeny. Philo Trans R Soc Lond B 348:405–421
Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD (2008) Sexual selection and adaptive evolution of mammalian ejaculate proteins. Mol Biol Evol 25:207–219
Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53
Soulsbury CD (2009) Ovulation mode modifies paternity monopolization in mammals. Biol Lett. doi:10.1098/rsbl.2009.0703
Stallman RR, Harcourt AH (2006) Size matters: the (negative) allometry of copulatory duration in mammals. Biol J Linn Soc 87:185–193
Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320
Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189
Acknowledgments
We thank Rob Freckleton for providing the R code for the PGLM and the three referees and the editor (Dave Hosken) for their valuable comments.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Soulsbury, C.D., Iossa, G. The impact of ovulation mode on sperm quantity and quality in mammals. Evol Ecol 24, 879–889 (2010). https://doi.org/10.1007/s10682-009-9344-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-009-9344-y