Skip to main content
SpringerLink
Log in

Factors predicting male fertilization success in an external fertilizer

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

In postcopulatory sexual selection both sperm competition and cryptic female choice are considered to be important selective agents, but their relative importance for male fertilization success has received little attention. We tested whether sperm quality, male spawning coloration, male heterozygosity, and genetic overlap with the female explained a male’s fertilization success in controlled in vitro fertilization competition trials between equal numbers of sperm from pairs of male Arctic charr (Salvelinus alpinus), an external fertilizer. Offspring were genotyped to determine each males’ share of paternity. The velocity of a male’s sperm relative to the velocity of the competing male’s sperm was the best predictor of male fertilization success. Yet, sperm velocity was not related to spawning coloration or male heterozygosity. In fact, the most brightly colored male in a pair had the lowest fertilization probability. This could result from cryptic female choice for pale males, but might rather be a result of paler males producing more competitive sperm than more colored males. Furthermore, the more microsatellite alleles a male shared with the female relative to the competing male, the higher fertilization success he had. We argue that this latter may be an effect of assortative cryptic female choice, which might prevent hybridization with sympatric Arctic charr morphs or one form of kin selection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ball MA, Parker GA (1996) Sperm competition games: external fertilization and “adaptive” infertility. J Theor Biol 180:141–150

    Article  PubMed  CAS  Google Scholar 

  • Bierne N, David P, Boudry P, Bonhomme F (2002) Assortative fertilization and selection at larval stage in the mussels Mytilus edulis and M-galloprovincialis. Evolution 56:292–298

    PubMed  Google Scholar 

  • Billard R (1988) Artificial-insemination and gamete management in fish. Mar Behav Physiol 14:3–21

    Article  Google Scholar 

  • Birkhead TR, Fletcher F (1995) Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proc R Soc Lond B Biol Sci 262:329–334

    Article  CAS  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, San Diego

    Google Scholar 

  • Birkhead TR, Pizzari T (2002) Postcopulatory sexual selection. Nat Rev Genet 3:262–273

    Article  PubMed  CAS  Google Scholar 

  • Birkhead TR, Moller AP, Sutherland WJ (1993) Why do females make it so difficult for males to fertilize their eggs. J Theor Biol 161:51–60

    Article  Google Scholar 

  • Birkhead TR, Buchanan KL, Devoogd TJ, Pellatt EJ, Szekely T, Catchpole CK (1997) Song, sperm quality and testes asymmetry in the sedge warbler. Anim Behav 53:965–971

    Article  Google Scholar 

  • Birkhead TR, Martinez 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

    Article  CAS  Google Scholar 

  • Blount JD, Moller AP, Houston DC (2001) Antioxidants, showy males and sperm quality. Ecol Lett 4:393–396

    Article  Google Scholar 

  • Cohen LB, Dearborn DC (2004) Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 68:1229–1236

    Article  Google Scholar 

  • Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-Plus. Wiley, West Succex

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, New Jersey

    Google Scholar 

  • Evans JP, Zane L, Francescato S, Pilastro A (2003) Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360–363

    Article  PubMed  CAS  Google Scholar 

  • Fabricius E (1953) Aquarium observations on the spawning behaviour of the char, Salmo alpinus. Rep Inst Freshw Res Drottningholm 34:14–48

    Google Scholar 

  • Figenschou L, Folstad I, Liljedal S (2004) Lek fidelity of male Arctic charr. Can J Zool-Revue Canadienne De Zoologie 82:1278–1284

    Article  Google Scholar 

  • Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    Article  PubMed  CAS  Google Scholar 

  • Folstad I, Skarstein F (1997) Is male germ line control creating avenues for female choice? Behav Ecol 8:109–112

    Article  Google Scholar 

  • Froman DP, Feltmann AJ, Rhoads ML, Kirby JD (1999) Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biol Reprod 61:400–405

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Geyer LB, Palumbi SR (2005) Conspecific sperm precedence in two species of tropical sea urchins. Evolution 59:97–105

    PubMed  Google Scholar 

  • Harper FM, Hart MW (2005) Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars. Biol Bull 209:113–126

    Article  PubMed  CAS  Google Scholar 

  • Harvey PH, May RM (1989) Copulation dynamics—out for the sperm count. Nature 337:508–509

    Article  PubMed  CAS  Google Scholar 

  • Hillgarth N, Ramenofsky M, Wingfield J (1997) Testosterone and sexual selection. Behav Ecol 8:108–109

    Article  Google Scholar 

  • Jonsson B, Jonsson N (2001) Polymorphism and speciation in Arctic charr. J Fish Biol 58:605–638

    Article  Google Scholar 

  • Kleven O, Jacobsen F, Robertson RJ, Lifield JT (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392

    Article  PubMed  Google Scholar 

  • Knudsen R, Curtis MA, Kristoffersen R (2004) Aggregation of helminths: the role of feeding behavior of fish hosts. J Parasitol 90:1–7

    Article  PubMed  Google Scholar 

  • Kortet R, Vainikka A, Rantala MJ, Taskinen J (2004) Sperm quality, secondary sexual characters and parasitism in roach (Rutilus rutilus L.). Biol J Linn Soc 81:111–117

    Article  Google Scholar 

  • Kupriyanova E, Havenhand JN (2002) Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa. Invertebr Reprod Dev 41:21–26

    Google Scholar 

  • Lahnsteiner F, Berger B, Weismann T, Patzner RA (1998) Determination of semen quality of the rainbow trout, Oncorhynchus mykiss, by sperm motility, seminal plasma parameters, and spermatozoal metabolism. Aquaculture 163:163–181

    Article  CAS  Google Scholar 

  • Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19:4293–4293

    Article  PubMed  CAS  Google Scholar 

  • Lehmann L, Perrin N (2003) Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am Nat 162:638–652

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Liljedal S, Folstad I (2003) Milt quality, parasites, and immune function in dominant and subordinate Arctic charr. Can J Zool-Revue Canadienne De Zoologie 81:221–227

    Article  Google Scholar 

  • Liljedal S, Folstad I, Skarstein F (1999) Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr. Proc R Soc Lond B Biol Sci 266:1893–1898

    Article  Google Scholar 

  • Locatello L, Rasotto MB, Evans JP, Pilastro A (2006) Colourful male guppies produce faster and more viable sperm. J Evol Biol 19:1595–1602

    Article  PubMed  CAS  Google Scholar 

  • Masvaer M, Liljedal S, Folstad I (2004) Are secondary sex traits, parasites and immunity related to variation in primary sex traits in the Arctic charr? Proc R Soc Lond B Biol Sci 271:S40–S42

    Article  Google Scholar 

  • McCullagh P, Nelder JA (1989) General linear models. Chapman & Hall, London

    Google Scholar 

  • Olsson M, Shine R, Madsen T, Gullberg A, Tegelstrom H (1996) Sperm selection by females. Nature 383:585–585

    Article  CAS  Google Scholar 

  • Palumbi SR (1999) All males are not created equal: Fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci USA 96:12632–12637

    Article  PubMed  CAS  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in insects. Biol Rev Camb Philos Soc 45:525–567

    Article  Google Scholar 

  • Parker GA (1990a) Sperm competition games—raffles and roles. Proc R Soc Lond B Biol Sci 242:120–126

    Article  Google Scholar 

  • Parker GA (1990b)) Sperm competition games—sneaks and extra-pair copulations. Proc R Soc Lond B Biol Sci 242:127–133

    Article  Google Scholar 

  • Peters A, Denk AG, Delhey K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120

    Article  PubMed  CAS  Google Scholar 

  • Pilastro A, Simonato M, Bisazza A, Evans JP (2004) Cryptic female preference for colorful males in guppies. Evolution 58:665–669

    PubMed  Google Scholar 

  • Rakitin A, Ferguson MM, Trippel EA (1999) Spermatocrit and spermatozoa density in Atlantic cod (Gadus morhua): correlation and variation during the spawning season. Aquaculture 170:349–358

    Article  Google Scholar 

  • Ratti O, Hovi M, Lundberg A, Tegelstrom H, Alatalo RV (1995) Extra-pair paternity and male characteristics in the Pied Flycatcher. Behav Ecol Sociobiol 37:419–425

    Article  Google Scholar 

  • R Core Development team (2004) R: A language and environment for statistical computing. R Foundation for Statistical Computing. In. Vienna, Austria

  • Rexroad CE, Coleman RL, Martin AM, Hershberger WK, Killefer J (2001) Thirty-five polymorphic microsatellite markers for rainbow trout (Oncorhynchus mykiss). Anim Genet 32:317–319

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sheldon BC (1994) Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B Biol Sci 257:25–30

    Article  Google Scholar 

  • Sherman CDH, Wapstra E, Uller T, Olsson M (2008) Males with high genetic similarity to the females sire more offspring in sperm competition in Peron’s tree frog Litoria peronii. Proc R Soc Lond B Biol Sci 275:971–978 DOI 10.1098/rspb.2007.1626

    Article  CAS  Google Scholar 

  • Sigurjonsdottir H, Gunnarsson K (1989) Alternative mating tactics of Arctic charr, Salvelinus Alpinus, in Thingvallavatn, Iceland. Environ Biol Fisches 26:159–176

    Article  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, New Jersey, USA

    Google Scholar 

  • Skarstein F, Folstad I (1996) Sexual dichromatism and the immunocompetence handicap: An observational approach using Arctic charr. Oikos 76:359–367

    Article  Google Scholar 

  • Skarstein F, Folstad I, Liljedal S (2001) Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Can J Zool-Revue Canadienne De Zoologie 79:271–278

    Article  Google Scholar 

  • Skarstein F, Folstad I, Liljedal S, Grahn M (2005) MHC and fertilization success in the Arctic charr (Salvelinus alpinus). Behav Ecol Sociobiol 57:374–380

    Article  Google Scholar 

  • Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53

    Article  PubMed  Google Scholar 

  • Stoltz JA, Neff BD (2006) Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J Evol Biol 19:1873–1881 DOI 10.1111/j.1420-9101.2006.01165.x

    Article  PubMed  CAS  Google Scholar 

  • Tarvin KA, Webster MS, Tuttle EM, Pruett-Jones S (2005) Genetic similarity of social mates predicts the level of extrapair paternity in splendid fairy-wrens. Anim Behav 70:945–955

    Article  Google Scholar 

  • Thornhill R (1983) Cryptic Female Choice and Its Implications in the Scorpionfly Harpobittacus-Nigriceps. Am Nat 122:765–788

    Article  Google Scholar 

  • Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027

    Article  PubMed  CAS  Google Scholar 

  • Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73

    Article  PubMed  CAS  Google Scholar 

  • Turner E, Montgomerie R (2002) Ovarian fluid enhances sperm movement in Arctic charr. J Fish Biol 60:1570–1579

    Article  Google Scholar 

  • Urbach D, Folstad I, Rudolfsen G (2005) Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus). Behav Ecol Sociobiol 57:438–444

    Article  Google Scholar 

  • Vaz Serrano J, Folstad I, Rudolfsen G, Figenschou L (2006) Do the fastest sperm within an ejaculate swim faster in subordinate than in dominant males of Arctic char? Can J Zool 84:1019–1024 DOI 10.1139/Z06-097

    Article  Google Scholar 

  • Westgaard JI, Klemetsen A, Knudsen R (2004) Genetic differences between two sympatric morphs of Arctic charr confirmed by microsatellite DNA. J Fish Biol 65:1185–1191

    Article  CAS  Google Scholar 

  • Yasui Y (1997) A “good-sperm” model can explain the evolution of costly multiple mating by females. Am Nat 149:573–584

    Article  Google Scholar 

Download references

Acknowledgements

Eirik Mack Eilertsen, Davnah Urbach, and Andreas Palmèn are acknowledged for enduring endless sessions of egg counting. E. M. Eilertsen is also the brain behind our ingenious, yet expensive, hatchery. Jon-Ivar Westgaard provided information about the microsatellite primers and PCR protocols. Jakob Lohm and Anne Grethe Hestnes never got tired of sharing their insights in various molecular biology techniques. Audun Stien introduced S. L. to quasibinomial tests and how to produce them, and additional plots, in the R software. Bård Jørgen Bårdsen was also very helpful teaching S. L. how to use R. Torkild Tveraa, Frode Skarstein, Jan T. Lifjeld and Anders P. Møller gave immensely improving comments to the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, University of Tromsø, 9037, Tromsø, Norway

    Ståle Liljedal, Geir Rudolfsen & Ivar Folstad

Authors
  1. Ståle Liljedal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geir Rudolfsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ivar Folstad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ivar Folstad.

Additional information

Communicated by C. St. Mary

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liljedal, S., Rudolfsen, G. & Folstad, I. Factors predicting male fertilization success in an external fertilizer. Behav Ecol Sociobiol 62, 1805–1811 (2008). https://doi.org/10.1007/s00265-008-0609-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-008-0609-1

Keywords

Search

Navigation