Abstract
Sperm competition theory predicts that males should tailor their investment in ejaculates according to the number of rival males competing to fertilize a female’s eggs. Research spanning several taxa supports this prediction by showing that males are often sensitive to the level of sperm competition and adjust their investment in sperm numbers accordingly. More recent work has revealed that males may also tailor the quality of sperm according to the number of males competing for fertilization. Here I test for both effects in guppies (Poecilia reticulata) in an experiment that simultaneously evaluates the risk and intensity models of sperm competition. The experiment determined whether male guppies adjust the number (stripped ejaculate size) and quality (sperm velocity and viability) of sperm that are primed over a 3-day period according to experimental changes in the perceived level of sperm competition. A total of 136 focal males were initially stripped of all retrievable sperm and assayed for these sperm traits before being allocated at random to one of four treatments simulating different levels of sperm competition risk and intensity. During the 3-day treatment phase, focal males had visual and olfactory access to a sexually receptive (initially virgin) female maintained with different numbers of stimulus males to simulate variation in the risk and intensity of sperm competition. Following this, males were assayed again for the sperm traits. Contrary to predictions, there was no significant change in any of the measured variables among treatments, although qualitatively the patterns for sperm velocity and viability did conform to expectation. The lack of any trend for the number of sperm primed was unequivocal and future work examining the effects of sperm competition on sperm production should focus on whether males differentially allocate sperm numbers among matings that differ in the level of sperm competition.

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Aspbury AS (2007) Sperm competition effects on sperm production and expenditure in sailfin mollies, Poecilia latipinna. Behav Ecol 18:776–780. doi:10.1093/beheco/arm044
Aspbury AS, Gabor CR (2004) Discriminating males alter sperm production between species. Proc Natl Acad Sci U S A 101:15970–15973. doi:10.1073/pnas.0405653101
Billard R (1969) La sperm spermatogenese de Poecilia reticulata. Ann Biol Anim Biochim Biophys 9:251–271. doi:10.1051/rnd:19690208
Billard R, Cosson MP (1990) The energetics of fish sperm motility. In: Gagnon C (ed) Controls of sperm motility: biological and clinical aspects. CRC, Boca Raton, pp 153–173
Birkhead TR, Møller AP (eds) (1998) Sperm competition and sexual selection. Academic, San Diego
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. doi:10.1098/rspb.1999.0843
Bozynski CC, Liley NR (2003) The effect of female presence on spermiation, and of male sexual activity on ’ready’ sperm in the male guppy. Anim Behav 65:53–58. doi:10.1006/anbe.2002.2024
Candolin U, Reynolds JD (2002) Adjustments of ejaculation rates in response to risk of sperm competition in a fish, the bitterling (Rhodeus sericeus). Proc. R. Soc. Lond. B.
Crow RT, Liley NR (1979) A sexual pheromone in the guppy, Poecilia reticulata (Peters). Can J Zool 57:184–188. doi:10.1139/z79-016
Denk AG, Holzmann A, Peters A, Vermeirssen ELM, Kempenaers B (2005) Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol 16:825–833. doi:10.1093/beheco/ari065
Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610. doi:10.1086/283938
Donoghue AM, Sonstegard TS, King LM, Smith EJ, Burt DW (1999) Turkey sperm mobility influences paternity in the context of competitive fertilization. Biol Reprod 61:422–427. doi:10.1095/biolreprod61.2.422
Dosen LD, Montgomerie R (2004) Mate preferences by male guppies (Poecilia reticulata) in relation to the risk of sperm competition. Behav Ecol Sociobiol 55:266–271. doi:10.1007/s00265-003-0710-4
Dziuk PJ (1996) Factors that influence the proportion of offspring sired by a male following heterospermic insemination. Anim Reprod Sci 43:65–68. doi:10.1016/0378-4320(95) 01463-2
Engqvist L, Reinhold K (2005) Pitfalls in experiments testing predictions from sperm competition theory. J Evol Biol 18:116–123. doi:10.1111/j.1420-9101.2004.00792.x
Evans JP, Magurran AE (1999) Male mating behaviour and sperm production characteristics under varying sperm competition risk in guppies. Anim Behav 58:1001–1006. doi:10.1006/anbe.1999.1212
Evans JP, Rutstein AN (2008) Postcopulatory sexual selection favours intrinsically good sperm competitors. Behav Ecol Sociobiol 62:1167–1173. doi:10.1007/s00265-008-0545-0
Evans JP, Pierotti M, Pilastro A (2003a) Male mating behavior and ejaculate expenditure under sperm competition risk in the eastern mosquitofish. Behav Ecol 14:268–273. doi:10.1093/beheco/14.2.268
Evans JP, Zane L, Francescato S, Pilastro A (2003b) Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360–363. doi:10.1038/nature01367
Fuller RC (1998) Sperm competition affects male behaviour and sperm output in the rainbow darter. Proc R Soc Lond B Biol Sci 265:2365–2371. doi:10.1098/rspb.1998.0585
Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative velocity is the primary determinant of fertilization success. Curr Biol 14:44–47
García-González F, Simmons LW (2005) Sperm viability matters in insect sperm competition. Curr Biol 15:271–275. doi:10.1016/j.cub.2005.01.032
García-González F, Simmons LW (2007) Shorter sperm confer higher competitive fertilization success. Evolution Int J Org Evolution 61:816–824. doi:10.1111/j.1558-5646.2007.00084.x
Gardiner DM (1978) Utilization of extracellular glucose by spermatozoa of two viviparous fishes. Comp Biochem Physiol 59A:165–168. doi:10.1016/0300-9629(78) 90200-1
Hain TJA, Neff BD (2007) Multiple paternity and kin recognition mechanisms in a guppy population. Mol Ecol 16:3938–3946. doi:10.1111/j.1365-294X.2007.03443.x
Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton
House CM, Simmons LW (2005) Relative influence of male and female genital morphology on paternity in the dung beetle Onthophagus taurus. Behav Ecol 16:889–897. doi:10.1093/beheco/ari066
Kilgallon SJ, Simmons LW (2005) Image content influences men’s semen quality. Biol Lett 1:253–255. doi:10.1098/rsbl.2005.0324
Koya Y, Iwase A (2004) Annual reproductive cycle and rate of the spermatogenic process in male mosquitofish Gambusia affinis. Ichthyol Res 51:131–136. doi:10.1007/s10228-004-0208-8
Kuckuck C, Greven H (1997) Notes on the mechanically stimulated discharge of spermiozeugmata in the guppy, Poecilia reticulata: a quantitative approach. Z Fischk 4:73–88
LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc R Soc Lond B Biol Sci 265:1997–2002. doi:10.1098/rspb.1998.0531
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Locatello L, Rasotto MB, Evans JP, Pilastro A (2006) Colourful male guppies produce faster and more viable sperm. J Evol Biol 19:1595–1602. doi:10.1111/j.1420-9101.2006.01117.x
Martel V, Damiens D, Boivin G (2008) Strategic ejaculation in the egg parasitoid Trichogramma turkestanica (Hymenoptera : Trichogrammatidae). Ecol Entomol 33:357–361. doi:10.1111/j.1365-2311.2007.00973.x
Matthews IM, Evans JP, Magurran AE (1997) Male display rate reveals ejaculate characteristics in the Trinidadian guppy Poecilia reticulata. Proc R Soc Lond B Biol Sci 264:695–700. doi:10.1098/rspb.1997.0099
Moore A, Waring CP (1999) Reproductive priming in mature male Atlantic salmon parr exposed to the sound of redd cutting. J Fish Biol 55:884–887. doi:10.1111/j.1095-8649.1999.tb00726.x
Nakatsuru K, Kramer DL (1982) Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216:753–755. doi:10.1126/science.216.4547.753
Neff BD, Pitcher TE, Ramnarine IW (2008) Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol Ecol 17:2975–2984. doi:10.1111/j.1365-294X.2008.03816.x
Nicholls EH, Burke T, Birkhead TR (2001) Ejaculate allocation by male sand martins, Riparia riparia. Proc R Soc Lond B Biol Sci 268:1265–1270. doi:10.1098/rspb.2001.1615
Olsén KH, Liley NR (1993) The significance of olfaction and social cues in milt availability, sexual hormones status, and spawning behaviour of male rainbow trout (Oncorhynchus mikiss). Gen Comp End 89:107–118. doi:10.1006/gcen.1993.1014
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev Camb Philos Soc 45:525–567. doi:10.1111/j.1469-185X.1970.tb01176.x
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, San Diego, pp 3–54
Parker GA, Ball MA, Stockley P, Gage MJG (1996) Sperm competition games: individual assessment of sperm competition intensity by group spawners. Proc R Soc Lond B Biol Sci 263:1291–1297. doi:10.1098/rspb.1996.0189
Parker GA, Ball MA, Stockley P, Gage MJG (1997) Sperm competition games: a prospective analysis of risk assessment. Proc R Soc Lond B Biol Sci 264:1793–1802. doi:10.1098/rspb.1997.0249
Pilastro A, Bisazza A (1999) Insemination efficiency of two alternative male mating tactics in the guppy (Poecilia reticulata). Proc R Soc Lond B Biol Sci 266:1887–1891. doi:10.1098/rspb.1999.0862
Pilastro A, Scaggiante M, Rasotto MB (2002) Individual adjustment of sperm expenditure accords with sperm competition theory. Proc Natl Acad Sci U S A 99:9913–9915. doi:10.1073/pnas.152133499
Pitcher TE, Rodd FH, Rowe L (2007) Sexual colouration and sperm traits in guppies. J Fish Biol 70:165–177. doi:10.1111/j.1095-8649.2006.01292.x
Pizzari T, Cornwallis CK, Froman DP (2007) Social competitiveness associated with rapid fluctuations in sperm quality in male fowl. Proc R Soc Lond B Biol Sci 274:853–860. doi:10.1098/rspb.2006.0080
Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289–310. doi:10.1007/s00265-006-0178-0
Radwan J (1998) Heritability of sperm competition success in the bulb mite, Rhizoglyphus robini. J Evol Biol 11:321–327. doi:10.1007/s000360050091
Robinson DM, Aspbury AS, Gabor CR (2008) Differential sperm expenditure by male sailfin mollies, Poecilia latipinna, in a unisexual-bisexual species complex and the influence of spermiation during mating. Behav Ecol Sociobiol 62:705–711. doi:10.1007/s00265-007-0495-y
Rudolfsen G, Figenschou L, Folstad I, Tveiten H, Figenschou M (2006) Rapid adjustments of sperm characteristics in relation to social status. Proc R Soc Lond B Biol Sci 273:325–332. doi:10.1098/rspb.2005.3305
Schaus JM, Sakaluk SK (2001) Ejaculate expenditures of male crickets in response to varying risk and intensity of sperm competition: not all species play games. Behav Ecol 12:740–745. doi:10.1093/beheco/12.6.740
Scott AP, Liley NR, Vermeirssen ELM (1994) Urine of reproductively mature female rainbow trout, Oncorhynchus mikiss (Walbaum), contains a priming pheremone which enhances plasma levels of sex steriods and gonadotropin II in males. J Fish Biol 44:131–147. doi:10.1111/j.1095-8649.1994.tb01590.x
Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53. doi:10.1016/j.tree.2004.10.011
Thomas ML, Simmons LW (2007) Male crickets adjust the viability of their sperm in response to female mating status. Am Nat 170:190–195. doi:10.1086/519404
Vladic T, Järvi T (2001) Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proc R Soc Lond B Biol Sci 268:1–7. doi:10.1098/rspb.2000.1322
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320. doi:10.1016/S0169-5347(02) 02533-8
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. doi:10.1016/j.theriogenology.2006.10.003
Wilson N, Tubman SC, Eady PE, Robertson GW (1997) Female genotype affects male success in sperm competition. Proc R Soc Lond B Biol Sci 264:1491–1495. doi:10.1098/rspb.1997.0206
Acknowledgements
I am grateful to Cameron Duggin for fish husbandry and performing the sperm viability assays and John Fitzpatrick and two anonymous reviewers for comments on a previous draft of the manuscript. This work was supported by a QEII Fellowship and Discovery Grant from the Australian Research Council.
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Evans, J.P. No evidence for sperm priming responses under varying sperm competition risk or intensity in guppies. Naturwissenschaften 96, 771–779 (2009). https://doi.org/10.1007/s00114-009-0529-6
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DOI: https://doi.org/10.1007/s00114-009-0529-6


